MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 409: 267–300, 2010
doi: 10.3354/meps08607
Published June 23
REVIEW
Chemical interactions between marine macroalgae
and bacteria
Franz Goecke, Antje Labes, Jutta Wiese, Johannes F. Imhoff*
Kieler Wirkstoff-Zentrum at the Leibniz Institute of Marine Sciences (IFM-GEOMAR), Am Kiel-Kanal 44, Kiel 24106, Germany
ABSTRACT: We review research from the last 40 yr on macroalgal–bacterial interactions. Marine
macroalgae have been challenged throughout their evolution by microorganisms and have developed in a world of microbes. Therefore, it is not surprising that a complex array of interactions has
evolved between macroalgae and bacteria which basically depends on chemical interactions of various kinds. Bacteria specifically associate with particular macroalgal species and even to certain parts
of the algal body. Although the mechanisms of this specificity have not yet been fully elucidated, ecological functions have been demonstrated for some of the associations. Though some of the chemical
response mechanisms can be clearly attributed to either the alga or to its epibiont, in many cases the
producers as well as the mechanisms triggering the biosynthesis of the biologically active compounds
remain ambiguous. Positive macroalgal–bacterial interactions include phytohormone production,
morphogenesis of macroalgae triggered by bacterial products, specific antibiotic activities affecting
epibionts and elicitation of oxidative burst mechanisms. Some bacteria are able to prevent biofouling
or pathogen invasion, or extend the defense mechanisms of the macroalgae itself. Deleterious
macroalgal–bacterial interactions induce or generate algal diseases. To inhibit settlement, growth
and biofilm formation by bacteria, macroalgae influence bacterial metabolism and quorum sensing,
and produce antibiotic compounds. There is a strong need to investigate the bacterial communities
living on different coexisting macroalgae using new technologies, but also to investigate the production, localization and secretion of the biological active metabolites involved in those possible ecological interactions.
KEY WORDS: Marine microoganisms · Defense · Beneficial communication · Biofilms ·
Oxidative burst · Antibiotic activity · Quorum sensing control
Resale or republication not permitted without written consent of the publisher
Over the past decades an intensive collaboration between chemists and ecologists has resulted in an increasing number of studies which have combined modern chemical techniques with ecologically relevant
experiments and theories (Pawlik 2000, Hay 2009).
Thousands of marine secondary metabolites have been
identified (Hay 1996). These compounds have been
shown to play a major role in mediation of diverse ecological interactions (Dworjanyn et al. 1999). Chemical
ecology has provided significant insights into the ecology, evolution and organization of marine populations,
communities, and also into the function of marine
ecosystems (Hay 2009). Selected aspects of marine
chemical ecology have been frequently reviewed with
a focus on specific taxonomic groups or systems (see
Hay 2009 and references therein). Thus, the establishment and composition of communities on surfaces and
on bodies of organisms (epibiosis, biofouling) and the
processes involved have been described by several authors (Wahl 1989, 2008, Krug et al. 2006, Qian et al.
2007, Harder 2009, Hay 2009). Sessile invertebrates
such as tunicates, cnidarians, bryozoans, barnacles,
and sponges were the model systems for these experiments. With respect to the chemical ecology of algae,
investigations were focused either on the capabilities of
the macroalgae for chemical defense against grazers or
*Corresponding author. Email: jimhoff@ifm-geomar.de
© Inter-Research 2010 · www.int-res.com
INTRODUCTION
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Mar Ecol Prog Ser 409: 267–300, 2010
on the communication between algae, e.g. for reproductive purposes (see Cronin & Hay 1996, Paul &
Puglisi 2004, Amsler 2008 and references therein,
Macaya & Thiel 2008, Paul & Ritson-Williams 2008). A
few interesting studies have been presented on fungi,
microalgae and protozoa as associates of macroalgae
(see Harder 1999, Hellio et al. 2002, Raghukumar 2002,
Kohlmeyer & Volkmann-Kohlmeyer 2003, Lam et al.
2008b). Detailed knowledge of the interaction of algae
with their associated microbes and among microbes on
algal surfaces and tissues is still lacking (Steinberg et
al. 1997, Steinberg & de Nys 2002, Kubanek et al. 2003).
Therefore, this review will focus on specific interactions
between macroalgae and bacteria.
(Holmström et al. 2002, Honkanen & Jormalainen
2005, Krug et al. 2006). Bacteria are dominant among
the primary colonizers of algal surfaces, followed by
diatoms and fungi (Qian et al. 2007, Lam et al. 2008a).
While some macroalgae are heavily colonized, other
algal species in the same habitat remain almost free of
epibionts. Such differences may even be found in
closely related species living in the same habitat, e.g.
in Fucus evanescens which show little epibiosis and F.
vesiculosus which are heavily fouled (Wikström &
Pavia 2004). This indicates the presence of an established antifouling defense in only some macroalgal
species (de Nys et al. 1993, Steinberg & de Nys 2002,
Bhadury & Wright 2004, Nylund & Pavia 2005) and, on
the other hand, species-specific contact mechanisms
between algae and bacteria.
COLONIZATION OF MACROALGAL SURFACES
BY MARINE MICROBES
Bacterial communities associated with macroalgae
Microbial epibiosis
Microorganisms are an essential component of
earth’s biosphere (Whitman et al. 1998). Their number
in aquatic environments is enormous. Seawater contains up to 107 viruses, 106 bacteria, 103 fungi, 103
microalgae, and 10 to 100 microscopic larvae and
spores per ml (Cole 1982, Jensen & Fenical 1994, Engel
et al. 2002, Harder 2009). The aquatic environment
favors the development of microbes and the formation
of biofilms on surfaces (Weinberger 2007). Macroalgae
are especially susceptible to epibiosis because they
live in an environment with strong competition for
space amongst benthic organisms (Hellio et al. 2001,
Harder et al. 2004, Potin et al. 2002, Lam et al. 2008b).
In addition, algal surfaces provide a habitat rich in
organic material. Macroalgae release large amounts
of organic carbon into the surrounding environment,
providing nutrients for microorganisms (Khailov &
Burlakova 1969, Kong & Chan 1979, Bouvy et al. 1986,
Armstrong et al. 2001, Lane & Kubanek 2008) and triggering chemotactic behaviour of bacteria (Bell &
Mitchell 1972, Paul & Puglisi 2004). Most primary
metabolites such as carbohydrates, amino acids, peptides, and proteins are inducers of microbial colonization (Steinberg et al. 2002). Hence, the surface of a
macroalga provides a protected microniche favorable
for bacterial colonization and reproduction (Byappanahalli et al. 2003, Beleneva & Zhukova 2006, Mahmud et
al. 2007, Englebert et al. 2008). For this reason, marine
macroalgae are continuously challenged by microorganisms as well as by grazers (Weinberger et al. 1997,
Bouarab et al. 2001).
The resulting marine microbial communities covering macroalga are complex and highly dynamic
ecosystems, consisting of a diverse range of organisms
Descriptive studies of bacteria isolated from the surface of macroalgae were reported as early as 1875
(Johansen et al. 1999). The interest in bacterial populations living in association with macroalgae has
increased during recent decades. We found 107 studies on bacterial communities associated to a total of 148
macroalgae (36 Chlorophyta, 46 Phaeophyceae, 55
Rhodophyta, 12 undetermined algae) within the last
40 yr (Table 1 & Appendix 1). Bacterial–macroalgal
associations were shown to be widely distributed in
marine habitats (Appendix 1). The number and complexity of these studies increased significantly during
the past decade. This increase can be attributed to the
combined use of improved methods in bacterial culture, microscopy and molecular biology (Fig. 1). However, many questions concerning the occurrence, distribution, persistence and ecological function of the
associated bacteria remain unresolved.
Fig. 1. Worldwide studies of bacterial communities associated
with macroalgae in the last 4 decades, showing the methodology used for the analysis. Data refers to Table 1 & Appendix 1
269
Goecke et al.: Marine macroalgal–bacterial interactions
Table 1. Macroalgae as source of new bacterial species. Quotation marks indicate proposed but not yet validated species
Macroalga
Bacterial species
Chlorophyta
Acrosiphonia sonderi (Kütz.) Kornm.
Algibacter lectus
Formosa agariphila
Mesonia algae
Pibocella ponti
Winogradskyella epiphytica
Zobellia russellii
Avrainvillea riukiuensis Yamada
Tenacibaculum amylolyticum
Capsosiphon fulvescens (Agardh) Setchell & Gardner Aequorivita capsosiphonis
Caulerpa sp.
Microbulbifer epialgicus
Enteromorpha linza (L.) J. Agardh
Erythrobacter longus
Ulva fenestrata Ruprecht
Algibacter lectus
Arenibacter certesii
Arenibacter palladensis
Maribacter ulvicola
Pseudozobellia thermophila
Roseivirga ehrenbergii
Ulvibacter litoralis
Ulva lactuca L.
Pseudoalteromonas ulvae
Heterokontophyta, Phaeophyceae
Chorda filum (L.) Stackhouse
Ecklonia kurome Okamura
Fucus evanescens C. Agardh
Fucus serratus L.
Kjellmaniella crassifolia Miyabe
Laminaria japonica Areschoug
Lessonia sp.
Padina sp.
Pocockiella sp.
Saccharina latissima (L.) Lane et al.
Undaria pinnatifida (Harvey) Suringar
Rhodophyta
Delesseria sanguinea (Huds.) Lamour
Gigartinaceae
Jania sp.
Polysiphonia japonica Harvey
Porphyra sp.
Unidentified red algae
Source
Nedashkovskaya et al. (2004e)
Nedashkovskaya et al. (2006a)
Nedashkovskaya et al. (2003)
Nedashkovskaya et al. (2005a)
Nedashkovskaya et al. (2005c)
Nedashkovskaya et al. (2004b)
Suzuki et al. (2001b)
Park et al. (2009)
Nishijima et al. (2009)
Shiba & Simidu (1982)
Nedashkovskaya et al. (2004e)
Nedashkovskaya et al. (2004a)
Nedashkovskaya et al. (2006b)
Nedashkovskaya et al. (2004d)
Nedashkovskaya et al. (2009)
Nedashkovskaya et al. (2005b)
Nedashkovskaya et al. (2004c)
Egan et al. (2001a)
Arenibacter latericius
Winogradskyella thalassocola
Croceitalea dokdonensis
Croceitalea eckloniae
Flagellimonas eckloniae
Bacillus algicola
Brevibacterium celere
Formosa algae
Pseudoalteromonas issachenkonii
Cellulophaga baltica
Cellulophaga fucicola
‘Fucobacter marina’
Pseudoalteromonas bacteriolytica
Winogradskyella eximia
Zobellia laminariae
Alteromonas atlantica
Roseibacillus ponti
Microbulbifer variabilis
Kiloniella laminariae
‘Gracilibacillus sp.’
Ivanova et al. (2001)
Nedashkovskaya et al. (2005c)
Lee et al. (2008b)
Lee et al. (2008b)
Bae et al. (2007)
Ivanova et al. (2004a)
Ivanova et al. (2004b)
Ivanova et al. (2004c)
Ivanova et al. (2002b)
Johansen et al. (1999)
Johansen et al. (1999)
Sakai et al. (2002)
Sawabe et al. (1998b)
Nedashkovskaya et al. (2005c)
Nedashkovskaya et al. (2004b)
Akagawa-Matsushita et al. (1992)
Yoon et al. (2008)
Nishijima et al. (2009)
Wiese et al. (2009a)
Tang et al. (2009)
Zobellia galactanovorans
Lacinutrix algicola
Lacinutrix mariniflava
Shewanella alga
Maribacter polysiphoniae
‘Phycisphaera mikurensis’
Luteolibacter algae
Barbeyron et al. (2001)
Nedashkovskaya et al. (2008)
Nedashkovskaya et al. (2008)
Simidu et al. (1990)
Nedashkovskaya et al. (2007)
Fukunaga et al. (2009)
Yoon et al. (2008)
Aeromicrobium tamlense
Agarivorans gilvus
Agrococcus jejuensis
Ferrimonas marina
Flavobacterium algicola
Koreibacter algae
Labedella gwakjiensis
Mesonia phycicola
Nitratireductor kimnyeongensis
Paracoccus zeaxanthinifaciens
Phycicoccus jejuensis
Phycicola gilvus
Lee & Kim (2007)
Du et al. (in press)
Lee (2008)
Katsuta et al. (2005)
Miyashita et al. (2010)
Lee & Lee (in press)
Lee (2007)
Kang & Lee (2010)
Kang et al. (2009)
Berry et al. (2003)
Lee (2006)
Lee et al. (2008a)
Unidentified macroalgae
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Mar Ecol Prog Ser 409: 267–300, 2010
Phylogenetic studies of epiphytic bacteria provided
an insight into the complex bacterial communities
associated with macroalgae (Penesyan et al. 2009).
Bacterial communities living on marine macroalgae
differ in number and composition of species from those
occurring in seawater (Kong & Chan 1979, Lemos et al.
1985, Mow-Robinson & Rheinheimer 1985, Johnson et
al. 1991, Steinberg et al. 2002, Longford et al. 2007). In
most cases, the epiphytic bacterial communities are
highly specific. Some microbes are found consistently
as epiphytes, e.g. Leucothrix mucor (Bland & Brock
1973). Recently, the variability and abundance of the
epiphytic bacterial community associated with Ulva
australis was investigated using molecular methods.
The results showed that members of the Alphaproteobacteria and the Bacteroidetes were a stable part of
the associated bacterial population (Tujula et al. 2010).
Bacterial–macroalgal associations comprised a number of new bacterial species, genera and even orders,
proving that macroalgae represent a distinct and rich
source of new microbial taxa (Genilloud et al. 1994).
From 36 macroalgal species, 56 new bacterial species
have been isolated (32% from Chlorophyta, 35% from
Phaeophyceae, 12% from Rhodophyta, and 21% from
undetermined algae) (Table 1).
Considering all available evidence, including our
own observations (Staufenberger et al. 2008, Lachnit et
al. 2009, Wiese et al. 2009a,b), it is reasonable to conclude that a highly specific association of bacterial
communities with marine macroalgae exists. It has
been proposed that the physiological and biochemical
properties of macroalgae predetermine the composition of the adhering microbial communities (Beleneva &
Zhukova 2006). Different species of marine algae growing under the same environmental conditions bear
different bacterial communities, varying in number and
composition. This assumption was investigated, using a
molecular approach, by Lachnit et al. (2009) regarding
the bacterial populations on Delesseria sanguinea, Fucus vesiculosus, Saccharina latissima (formerly Laminaria saccharina), and Ulva compressa growing in 2 different habitats. In that study, it was demonstrated that
bacterial communities derived from macroalgae belonging to the same species but originating from a
different habitat were more similar than those from different species inhabitating the same ecological niche.
Similar results were obtained by Nylund et al. (2010),
who analyzed 2 localities on the west coast of Sweden
with respect to the bacteria associated with the red
macroalgal species Bonnemaisonia asparagoides, Lomentaria clavellosa and Polysiphonia stricta.
In general, a stable association between host and
microorganisms is observed (Kong & Chan 1979, Shiba
& Taga 1980, Lewis et al. 1985, Johnson et al. 1991);
however, over the seasons or over the life span of the
basibiont the composition of the bacterial communities
may change (Laycock 1974, Hornsey & Hide 1976a,
Sakami 1996, Staufenberger et al. 2008). This has been
demonstrated for bacteria associated with Ascophyllum nodosum, Fucus vesiculosus, Sargassum natans
and Ulva australis (Sieburth & Conover 1965, Sieburth
& Tootle 1981, Hellio et al. 2004, Tujula et al. 2010).
Furthermore, it was reported that the composition of
the bacterial communities varies on different parts of
the thallus, e.g. for Ascophyllum nodosum (Cundell et
al. 1977), Chara vulgaris (Ariosa et al. 2004), and Saccharina latissima (Staufenberger et al. 2008) (Fig. 2). In
addition to different structural features of the specific
parts of the algal thallus, these differences may be
explained by a lack of vascular connections in the algal
tissue and by the resulting deficit in efficient resource
translocation (Honkanen & Jormalainen 2005). Various
biological activities (for example antibacterial and
antiherbivory activities) were found in extracts from
different parts of macroalgae which was shown by
unequal concentrations of the different secondary
metabolites throughout the thallus (Hornsey & Hide
1976b, Meyer & Paul 1992, Vlachos et al. 1999, FreilePelegrin & Morales 2004, Macaya et al. 2005). This
effect was shown for a number of metabolites, such as
soluble phlorotannins and halogenated organic compounds (Mehrtens & Laturnus 1997, Koivikko et al.
2005). In the brown alga Dictyota ciliolata, for example, the secondary metabolites pachydictyol A, dictyol
B acetate, dictyodial, and sterols were shown to be present in higher concentrations in older, less palatable
tissues than in apical meristem (Cronin & Hay 1996).
The same phenomenon was observed in the red
macroalga Neorhodomela larix regarding its content of
bromophenols such as lanosol (Phillips & Towers 1982,
Carlson et al. 1989). Therefore, different allocation and
concentration of the chemical compounds may lead to
different microbial communities at the different parts
of macroalgae (Fig. 2).
Although some of the bacterial–algal interactions
have been discussed earlier, the ecological relevance
of most naturally occurring bacterial communities on
macroalgae remains unclear and in most cases the bacterial species involved have not yet been identified
(Duan et al. 1995, Ivanova et al. 2002a). For example,
many coenocytic green macroalgae such as Caulerpa,
Codium, Bryopsis and Penicillus spp. have been shown
to harbour endosymbiotic bacteria, as shown by microscopic studies (Burr & West 1970, Turner & Friedmann
1974, Dawes & Lohr 1978, Rosenberg & Paerl 1981).
However, only in Caulerpa taxifolia could it be shown,
using molecular approaches, that Herbaspirillum sp.related bacteria are host-specific endosymbionts
(Meusnier et al. 2001, Delbridge et al. 2004). The characterization of microorganisms associated with algae is
Goecke et al.: Marine macroalgal–bacterial interactions
still at an early stage of development and detailed molecular studies on microbial communities associated
with macroalgae are rare (Staufenberger et al. 2008).
Studies of macroalgal–microbial interactions have
lagged, mainly for methodological reasons (Largo et al.
1997, Kohlmeyer & Volkmann-Kohlmeyer 2003). Suitable tools for the analysis of epiphytic bacterial communities including culture-independent approaches
were not available until molecular techniques were
introduced to this field of research (Fig. 1) (Ashen &
Goff 1998, 2000, Meusnier et al. 2001, Ohkubo et al.
2006, Tujula et al. 2006, Weinberger 2007, Burke et al.
2009). Until now, most of the available information
about bacterial–macroalgal interactions was obtained
from culture studies (Fisher et al. 1998, Skovhus et al.
2004). If we consider that only ca. 1 to 10% of the associated bacteria have been cultivated (Jensen et al.
1996), it is reasonable to assume that most of the ecologically relevant bacteria are not known so far. The
same is true for their possible susceptibility to naturally
Fig. 2. Saccharina latissima. A brown
alga with scanning electron micrographs
(SEM) of associated epiphytic bacteria
growing on 3 different parts. (a) Older
thallus. Disrupted mucilage and single
rod-form bacteria are visible. (b) Young
thallus. Cocci, rods and spirilli are present. (c) Rhizoid. Cocci in clusters are
present. (Modified after Staufenberger
et al. 2008). Courtesy of Dr. Rolf Schmaljohann (IFM-GEOMAR)
271
released algal metabolites (Paul et al. 2006). However,
an increasing number of results demonstrate that
chemical interactions determine the bacterial–algal
relationships. The substances on the surface of a
macroalga include exuded secondary metabolites and
extracellular exopolymers. As soon as algal metabolites are degraded by the associated bacteria, the
chemical cocktail may be further enriched (Lachnit et
al. 2010). Many bacterial taxa obtained from algal tissue are able to degrade sugars produced by algae,
such as alginate, cellulose and manitol (Table 2). They
are considered to be involved in the decay process of
algal fronds (Johnson et al. 1971, Lewis et al. 1985,
Uchida & Nakayama 1993, Jensen et al. 1996, Sakami
1999, Ivanova et al. 2005). Probably, this is one reason
for specific macroalgal–bacterial interactions (Kong &
Chan 1979, Lu et al. 2008).
Numerous studies on antifouling activity of extracts
and isolated substances from macroalgae have shown
that algae are a rich source of bioactive compounds
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Mar Ecol Prog Ser 409: 267–300, 2010
Table 2. Enzymatic activities detected in marine bacteria that are relevant to the degradation of macroalgal cell walls. *Bacteria
isolated from algae
Enzyme
Bacteria
Source
Agarases
Acinetobacter sp.
Agarivorans spp.
Alterococcus spp.
Alteromonas spp.*
Bacillus sp.
Cellulophaga baltica*, C. fucicola*
Cytophaga spp.
Flavobacterium spp
Glaciecola agarilytica
Marinilabilia spp.
Microbulbifer spp.*
Microscilla spp.
Phycisphaera mikurensis*
Pseudoalteromonas agarivorans*
P. antarctica*, P. gracilis*
Pseudomonas atlantica*
Persicobacter spp.
Pseudozobellia thermophila*
Saccharophagus spp.
Thalassomonas spp.
Vibrio spp.*
Zobellia galactanovorans*, Z. laminariae*, Z. russellii*
Alteromonas fortis
Cytophaga (Cytophaga drobachiensis*)
Marinilabilia spp.
Microbulbifer sp.* CMC-5
Microbulbifer elongates*
Pseudoalteromonas carrageenovora*
Zobellia galactanivorans*
Alcaligenes spp.*
Alginomonas spp.
Alginovibrio (A. aquatilis)
Alteromonas atlantica*, A. carrageenovora*, A. sp.*
Cytophaga diffluens
Deleya marina*
Flavobacterium sp.*
Glaciecola sp.
Gracilibacillus spp.* G halotolerans*
Halomonas marina, H. sp. AW4*
Moraxella sp.*
Ochrobactrum sp.*
Pseudoalteromonas sp.*
Pseudomonas alginovora*
Streptomyces sp. ALG-5*
Vibrio spp. (V. fischeri*, V. harveyi*)
Arenibacter spp.*
Flavobacterium algicola*
Fucobacter marina*
Fucophilus fucoidanolyticus*
Gramella sp.
Maribacter sp.
Mesonia algae*
Pseudoalteromonas citrea*
P. issachenkonii*
Sphingomonas paucimobilis
Vibrio sp.
Zobellia sp.*
Alteromonas sp. SN-1009
Mariniflexile fucanivorans
Aeromonas sp. F-25
Bacillus subtilis
Pseudomonas sp. PT-5*
Streptomyces lividans
Vibrio sp.*
Acinetobacter spp.
Alteromonas spp.
Flavobacterium spp.
Pseudoalteromonas sp.*
Vibrio spp.*
Yaphe (1957), Quatrano & Caldwell (1978), Vera
et al. (1998), Allouch et al. (2003), Johansen et al.
(1999), Romanenko et al. (2003), Schroeder et al.
(2003), Nedashkovskaya et al. (2004b), Jam et al.
(2005), Michel et al. (2006), and literature therein,
Flament et al. (2007), Yong et al. (2007), Fukunaga et al. (2009), Nedashkovskaya et al. (2009),
Fu & Kim (2010)
Carrageenases
Alginases
Fucoidanases
Fucanases
Mannanase
Cellulases
& pectinases
Yaphe & Baxter (1955), Sarwar et al. (1983), Potin
et al. (1991), Nakagawa & Yamasato (1996),
Barbeyron et al. (1998, 2000), Michel et al. (2006),
and literature therein, Jam et al. (2005), Khambhaty et al. (2007), Jonnadula et al. (2009)
Ando & Inoue (1961), Davidson et al. (1976),
Stevens & Levin (1977), Quatrano & Caldwell
(1978) and references therein, Preston et al.
(1986), Boyen et al. (1990), Brown et al. (1991),
Tseng et al. (1991), Akagawa-Matsushita et al.
(1992), Ramaiah & Chandramohan (1992),
Sawabe et al. (1992), Uchida & Nakayama (1993),
Uchida et al. (1995), Sakami (1999), Sawabe et al.
(1997, 1998a), Kraiwattanapong et al. (1999),
Ivanova et al. (2002a,b), Uchida et al. (2002),
Wang et al. (2006), Sawabe et al. (2007), An et al.
(2008, 2009), Tang et al. (2008), Zhou et al.
(2008), Kim et al. (2009), Tang et al. (2009)
Furukawa et al. (1992), Bakunina et al. (2000,
2002), Ivanova et al. (2002a), Sakai et al. (2002,
2003, 2004), Kusaykin et al. (2006), Urvantseva et
al. (2006), Kim et al. (2008), Miyashita et al. 2010)
Colin et al. (2006), Descamps et al. (2006),
Barbeyron et al. (2008)
Yamaura et al. (1990), Moreira & Filho (2008),
Tanaka et al. (2009)
Araki et al. (1992), Ramaiah & Chandramohan
(1992), Yamasaki et al. (1998), Ivanova et al.
(2002a), Yoshimura et al. (2006)
Goecke et al.: Marine macroalgal–bacterial interactions
against colonizing organisms (see section below on
antibiotic activities of macroalga-associated bacteria
and Table 5) (Steinberg et al. 1998, Bhadury & Wright
2004, Dobretsov et al. 2006b, Lane & Kubanek 2008,
and references therein, Nylund et al. 2008). In addition
to being defense mechanisms, these substances can
trigger specific interactions between macroalgae and
colonizers. Macroalgae without their own chemical
defense are considered to rely on the secondary metabolites produced by their associated bacteria (Holmström et al. 1992, Egan et al. 2000 and references
therein). Dobretsov & Qian (2002) showed that the
antifouling mechanisms of Ulva reticulata (Chlorophyta) rely not only on compounds released from the
alga itself but also on those produced by epibiotic bacteria, e.g. by a thallus-associated Vibrio sp. (Harder et
al. 2004).
Fouling organisms have negative effects on host
growth and reproduction. Hence, evolutionary pressure on marine macroalgae has favored the development of mechanisms to defend their surfaces against
biofilms (Wahl 1989, Steinberg & de Nys 2002).
DETRIMENTAL BACTERIAL–MACROALGAL
INTERACTIONS — DISEASES
Quantification of bacterial epiphytes on different
marine macrophytes showed that healthy individuals
carry 104 to 7 ×105 bacteria per gram algal fresh weight
(Laycock 1974, Jensen et al. 1996). By contrast, the
number of bacteria and saprophytes was increased by
more than 2 orders of magnitude (440 times) in diseased macroalgae (Weinberger et al. 1994). Despite
some beneficial aspects of epibiosis (see Wahl 1989,
2008), biofilm formation produces a permanent threat
to macroalgae (Steinberg et al. 1997, Potin et al. 2002,
Honkanen & Jormalainen 2005, Nylund & Pavia 2005,
Medeiros et al. 2007). Epibiosis may lead to increased
hydrodynamic drag on the basibiont. It may reduce the
buoyancy and elasticity of the tissue, attract grazers,
and thereby increase tissue loss of the host or may
even result in its destruction. In additon, bacteria compete with algae for nutrients and may even be more
efficient in uptake and assimilation of nutrients
(Berland et al. 1972). Biofilms may also inhibit gaseous
exchange as well as reducing incident light and
thereby decrease photosynthetic activity (Provasoli &
Pintner 1980, Sieburth & Tootle 1981, Wahl 1989, 2008,
Steinberg et al. 1997, Mindl et al. 2005). Bacterial biofilms may enhance the attachment and growth of a
range of other fouling organisms, such as diatoms,
invertebrate larvae, and algal spores (Joint et al. 2002,
Tait et al. 2005, Huggett et al. 2006). The host may
even be damaged directly by the bacterial community
273
due to the production of toxins, digestive enzymes,
inhibitors or waste products (Weinberger et al. 1997,
Ivanova et al. 2002a,b, Patel et al. 2003, Rao et al. 2006)
(Table 2).
Microorganisms that are common on the surface of
macroalgae might become detrimental if they are able
to enter the algal tissue. In order to attack the frond tissues, a pathogen must penetrate the cuticle layers of
the macroalga (Craigie et al. 1992). Algal cell walls and
cuticles contain a great diversity of polysaccharides,
which make them chemically and structurally more
complex and heterogeneous than those of terrestrial
plants (Polne-Fuller & Gibor 1987). Bacteria capable of
degrading the macroalgal cell wall are important factors for the damage of algal tissue and provide an
entrance for pathogenic and opportunistic bacteria
(Buschmann et al. 1997, Ivanova et al. 2005). Not only
bacteria but also algal endophytes are able to breach
the cuticula and cell wall and facilitate secondary
infections. An example of this is the green endophytic
alga Acrochaete operculata. It causes cellular damage
to Chondrus crispus (Rhodophyta) and leads to secondary bacterial infections by facultative pathogens
from the Cytophaga/Flavobacterium group (Correa &
McLachlan 1994, Craigie & Correa 1996). Vibrio species have been reported as one of the opportunistic
pathogens from diseased Porphyra and Laminaria
fronds (Wang et al. 2008). Usually, the secondary bacterial infection contributes to further disintegration of
the infected tissue, finally leading to thallus rupture.
Bacterial decomposition of dead and drying macroalgae on the beaches is rapid, indicating the abundant
presence of decomposing bacteria in the living algal
community (Uyenco et al. 1981, Delille & Perret 1991).
A large proportion of bacteria in coastal waters are
able to decompose macroalgal thalli (Uchida 1995,
Uchida et al. 2002, Yoshimura et al. 2006). As bacteria
are able to utilize algal nutrients selectively, they play
a key role in the biotransformation (Chesters et al.
1956, Ramaiah & Chandramohan 1992). They release a
variety of compounds which are subsequently used by
other organisms (Yaphe & Baxter 1955, Yaphe 1962,
Dimitrieva & Dimitriev 1996, Sawabe et al. 1998b,
Ivanova et al. 2002a,b, Sakai et al. 2002, Romanenko et
al. 2003). Biotransformation and nutrient recycling is
initiated by bacterial enzymes such as cellulases, alginases, fucoidanases, pectinases and agarases. Many of
these enzymes have biotechnological applications
(Yamasaki et al. 1998, Wong et al. 2000, Descamps et
al. 2006, Wang et al. 2006, Kim et al. 2009). Despite the
large number of associated bacteria, these lytic activities have been found only in a small number of genera
(Table 2).
Pathogenic bacteria in host-associated biofilms
cause significant mortality to their hosts or cause sig-
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Mar Ecol Prog Ser 409: 267–300, 2010
nificant degradation of algal host tissue (Littler & Littler 1995, Correa & Sánchez 1996, Steinberg et al.
1997). Despite the prevalence of microbes in the ocean
and the nature of pathogen-borne epidemics, diseases
among marine macroalgae are rare (Table 3). This is
even more remarkable, considering that algae do not
have cell-based immune systems (Potin et al. 1999,
Kubanek et al. 2003). However, evidence for induced
defense reactions of algae upon pathogen recognition
is emerging (Potin et al. 2002, Steinberg & de Nys
2002, Weinberger et al. 2005, Weinberger 2007).
Bacterial infections of macroalgae may cause obvious
but non-necrotic changes in morphology, appearance
of holes in the thallus, or discolorations causing light or
dark areas. It is also possible that they may not affect
the visible appearance of the alga at all (Andrews 1976,
Uyenco et al. 1981, Correa 1997). The association of
bacteria with abnormal tissue growth (galls) on marine
macroalgae is well known and has been found in more
than 20 species of red and brown macroalgae (McBride
et al. 1974, Tripodi & Beth 1976, Tsekos 1982, Apt 1988
and literature therein). For example, bacterial symbionts of the Roseobacter group are able to cause such
gall formations in the red macroalga Prionitis spp.
(Ashen & Goff 2000). The metabolic consequences of
gall formation for the macroalgae and its bacterial inhabitants remain unknown. But apparently the hypertrophic growth of gall-induced algal cells provides a
suitable microhabitat for proliferation of the ‘symbiont’
(Apt & Gibor 1989, Ashen & Goff 1998).
Table 3. Macroalgal diseases caused by bacteria. (–) not specified
Macroalgae
Disease
Heterokontophyta, Phaeophyceae
Cystoseira nodicaulis
–
Pathogen
Source
Unidentified Proteobacteria
Pellegrini & Pellegrini (1982)
Laminaria japonica
Hole-rotten disease
Pseudoalteromonas,
Vibrio, Halomonas
Wang et al. (2008)
Laminaria japonica
Summer sporelings
disease
Micrococcus sp.
Wu (1990)
Laminaria japonica
Red spot disease
Pseudoalteromonas
bacteriolytica
Ezura et al. (1988), Sawabe et al.
(1998b), Yumoto et al. (1989a,b)
Laminaria japonica
Spot-wounded fronds
Pseudoalteromonas elyakovii Sawabe et al. (2000)
Undaria pinnatifida
Green decay diseases
Vibrio logei
Jiang et al. (1997)
Rhodophyta
Chondrus crispus
–
Cytophaga/Flavobacterium
group
Correa & McLachlan (1994),
Craigie & Correa (1996)
Gracilaria conferta
–
Cytophaga/Flavobacterium
and Vibrio group
Weinberger et al. (1997),
Weinberger & Friedlander (2000b)
Gracilaria gracilis
–
Undetermined bacteria
Jaffray & Coyne (1996)
Gracilaria gracilis
–
Pseudoalteromonas gracilis
Schroeder et al. (2003)
Gracilaria sp.
Rotten thallus syndrome
Vibrio sp.
Lavilla-Pitogo (1992)
Gracilaria verrucosa
Rotten thallus syndrome
Vibrio sp.
Beleneva & Zhukova (2006)
Hydrolithon, Sporolithon,
Lithophyllum,Titanoderma
and other coralline algae
Thallus holes
Plectonema terebrans
Ghirardelli (1998, 2002), Tribollet
& Payri (2001)
Kappaphycus alvarezii
Ice-ice whitening
Cytophaga-Flavobacterium
group-Vibrio group
Largo et al. (1995, 1999),
Vairappan et al. (2008)
Mazzaella laminarioides
Deformative disease
Pleurocapsa sp.
Buschmann et al. (1997),
Correa et al. (1993)
Porolithon onkodes
and other coralline algae
Coralline lethal orange
disease (CLOD)
–
Aeby (2007), Littler & Littler
(1994, 1995)
Porphyra leucosticta
White rot disease
Vibrio sp.
Tsukidate (1977, 1983)
Porphyra leucosticta
Suminori
Flavobacterium sp.
Kusuda et al. (1992)
Porphyra yezoensis
Green spot rotting
Vibrio sp., Pseudomonas sp.
Fujita et al. (1972), Nakao
et al. (1972)
Porphyra yezoensis
Anaaki
Flavobacterium sp.
Sunairi et al. (1995)
Goecke et al.: Marine macroalgal–bacterial interactions
BENEFICIAL BACTERIAL–MACROALGAL
INTERACTIONS
The role of epiphytic bacteria in maintaining the
health of the host has received little attention. Though
beneficial associations between bacteria and their host
have been identified (Cole 1982, Weinberger et al.
1997, Dobretsov & Qian 2002, Rao et al. 2006), the
advantages for algae are less obvious (Marshall et al.
2006).
Nutritional aspects and growth factors
Beneficial relationships may be based on the algal
capacity to produce organic compounds and oxygen
which are utilized by bacteria (Brock & Clyne 1984,
Coveney & Wetzel 1989). In turn, bacteria mineralize
organic substrate, supplying the algae with carbon
dioxide, minerals and growth factors (Croft et al. 2005,
2006). Several studies indicated that marine epiphytic
bacteria are important sources of fixed nitrogen for
algae. Diverse epiphytic Cyanobacteria (Calothrix sp.,
Anabaena sp., and Phormidium sp.) that fix nitrogen
and supply it to Codium species (Chlorophyta) have
been described from certain locations (Dromgoole et
al. 1978, Rosenberg & Paerl 1981). Another nitrogen
fixer, Dichothrix fucicola, was located in association
with populations of Sargassum natans and S. fluitans
in the Sargasso Sea and the Gulf Stream (Carpenter
1972, Carpenter & Cox 1974). The nitrogen supply of
Caulerpa taxifolia is provided by an endosymbiotic
bacterium from the Agrobacterium-Rhizobium group,
living in the algal rhizoids (Chisholm et al. 1996). A
significant nitrogenase activity was attributed to the
nitrogen-fixing Azotobacter sp., present on the
macroalga Codium fragile subsp. tomentosoides (Head
& Carpenter 1975), indicating nitrogen fixation within
the association.
These associations secure the supply of dinitrogen to
the macroalgae and might be one of the reasons for the
successful invasion of these noxious macroalgae (like
Caulerpa taxifolia or Codium fragile) into oligotrophic
environments (Chisholm et al. 1996). Indeed, in other
aquatic environments, some epiphytic Cyanobacteria
like Nostoc sp., Calothrix sp. and Anabaena sp., living
on the green macroalga Chara vulgaris seem to be the
main nitrogen contributors (Ariosa et al. 2004).
In addition to nitrogen fixation, microbes play a role
in the protection of the macroalga against toxic compounds such as heavy metals (Riquelme et al. 1997,
Dimitrieva et al. 2006) or crude oil (Semenova et al.
2009). Microorganisms are able to detoxify, for example, heavy metals by precipitation, adsorption, or transformation to less toxic forms (Yurkov & Beatty 1998).
275
Bacteria also supply macroalgae with growth factors,
e.g. by involvement in the production and turnover
of various phytohormones and biostimulators of cell
growth and development (Berland et al. 1972, Bolinches et al. 1988, Meusnier et al. 2001). For example,
a favorable growth-promoting effect by the bacterium
Pseudoalteromonas porphyrae was observed on Laminaria japonica (Dimitrieva et al. 2006). Plant hormone
production seems to be widespread in various genera
of marine bacteria. Maruyama et al. (1990) demonstrated that bacteria produce more cytokinin-type and
auxin-type hormones when associated with macroalgae as compared to planktonic bacteria. Previous
studies showed the ability of bacteria living on Ulva
spp. (formerly Enteromorpha) to convert tryptophan
into the phytohormone indole-3-acetic acid (IAA)
(Fries 1975). In the macroalga Prionitis lanceolata, the
gall formation mentioned above is associated with a
bacterium of the Roseobacter group. IAA is overproduced in those algal galls in comparison to the rest of
the thallus. Although the role of the bacterium in the
physiology of the macroalga is not well understood, a
coevolution has been suggested (Ashen et al. 1999,
Ashen & Goff 2000).
Impact on macroalgal morphology
Beside nutrititional and growth promoting effects,
bacteria affect the morphology and life cycle of macroalgae. Marine foliaceous green macroalgae such as
Ulva spp. drastically lose their typical morphology
when cultured aseptically (Fries 1975, Provasoli & Pintner 1980, Tatewaki et al. 1983). This phenomenon was
also observed in the red macroalgae Dasya pedicellata
C. Agardh and Polysiphonia urceolata (Dillwyn) Greville (Provasoli & Pintner 1972). Addition of adequate
marine bacteria or their culture filtrates restored the
typical morphology of these macroalgae (Nakanishi et
al. 1999). Actually, morphogenesis in such macroalgae
(Ulvaceae and Monostromaceae) is controlled by a restricted group of bacteria of the Bacteroidetes phylum,
mainly Cytophaga and Flavobacterium spp. (Hanzawa
et al. 1998, Nakanishi et al. 1999, Matsuo et al. 2005,
Marshall et al. 2006). Furthermore, morphogenic effects on macroalgae were also demonstrated for members of the genera Caulobacter, Vibrio, Pseudomonas,
Deleya, Escherichia and some Gram-positive bacteria
(Nakanishi et al. 1996). These bacteria lose their ability
to induce morphogenic effects when grown alone for
several generations in marine media containing rich
organic sources, but regain it under co-cultivation with
Ulva in synthetic mineral media. Both ‘partners’ apparently depend on the metabolites produced by the other
(Provasoli & Pintner 1980).
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Mar Ecol Prog Ser 409: 267–300, 2010
Thallusin was the first compound identified to
induce thallus differentiation in macroalgae. It was
produced from an epiphytic marine bacterium isolated
from the alga Monostroma sp. (Matsuo et al. 2003). In
order to maintain the common algal morphology, this
compound has to be constantly supplied by the bacterium. Thallusin exemplifies a fundamental symbiotic
chemical communication between macroalgae and
epiphytic bacteria in the marine environment (Matsuo
et al. 2005). However, the mechanism of modulation of
algal morphology by thallusin is not yet understood
(Marshall et al. 2006).
Effect on spore germination and macroalgal
colonization
Recently, it was discovered that bacterial biofilms
play a role in spore germination and subsequent colonization of new substrates by algae. A set of diverse
bacterial species isolated from marine surfaces colonized by Ulva spp. either stimulated or inhibited the
zoospore settlement of this green macroalgae (Patel
et al. 2003, Tait et al. 2005). Phylogenetic analysis
revealed that the isolated bacteria belonged to the
Gammaproteobacteria, the Cytophaga-FlavobacteriaBacteroidetes group and Alphaproteobacteria. Most of
these microorganisms revealing stimulating effects
were strains of Vibrio and Shewanella species. Effects
on spore settlement were strain- but not species-specific, and the activity varied with the age of the biofilm.
A positive correlation between zoospore settlement of
Ulva linza and bacterial biofilm density indicates the
important role of bacterial biofilms in the development
of algal communities (Marshall et al. 2006).
It appears that these are not isolated cases. Of the
192 bacterial strains isolated from the surfaces of seaweeds from China, 63 isolates were shown to be
inhibitory against the settlement of algal spores (Ma et
al. 2009). Also, a number of diverse bacterial metabolites affect the germination of spores of various
macroalgae (Egan et al. 2001b, Matsuo et al. 2003,
Dimitrieva et al. 2006) (Table 4). For example, an
antialgal peptide that inhibited spore germination was
produced by Pseudoalteromonas tunicata isolated
from Ulva australis (Egan et al. 2001b). The fatty acids
cis-9-oleic acid and 2-hydroxymyristic acid produced
by the bacterium Shewanella oneidensis (Bhattarai et
al. 2007) as well as a peptidic compound produced by
the bacterium Alteromonas sp. (isolated from the red
alga Rhodymenia sp.) exhibited activity against spores
of U. lactuca (Silva-Aciares & Riquelme 2008).
As mentioned, bacterial biofilms play an important
role in initiation of colonization processes. A preferential settlement of spores on specific bacterial biofilms
producing morphogenic compounds may facilitate a
close association of the developing macroalgae with
these specific bacterial ‘episymbionts’ (Joint et al. 2002,
Patel et al. 2003). As we discuss later, these epibionts
play a protective role by releasing compounds into the
surrounding seawater that prevent extensive biofouling of the surface or act against microbial pathogens
(Armstrong et al. 2001, Wiese et al. 2009b).
CHEMICAL INTERACTIONS
Since the 1970s it has been known that chemical
compounds are the basis of many aspects of communication and molecular interaction between aquatic
organisms (Bhakuni & Silva 1974, Scheuer 1978, Hay
2009). However, studies on these chemical interactions
within marine communities are relatively new as compared to the analyses of feeding relationships (Paul &
Puglisi 2004). More intense investigations of the large
variety of interactions between hosts and microbes and
between different microbes should reveal the different
communication pathways, which include the production of defensive or deterrent compounds, pheromones, attractants and other signal substances. Some
of these compounds act in a general way while others
have highly specific modes of action (Davies et al.
1998, Rasmussen et al. 2000, Da Gama et al. 2002).
Chemically mediated interactions like fertilization,
allelopathy, and prey detection between macroalgae
and other marine organisms fundamentally depend on
the sensing of chemicals at or near surfaces (Steinberg
& de Nys 2002). It has been demonstrated that the
microbial colonization of various host organisms might
be controlled by host-derived molecules (Wahl et al.
1994, Rao & Fujita 2000). However, little is known
about the potential role of secondary metabolites in the
regulation and development of associations. Other
chemically mediated types of microbial behaviors such
as chemotaxis, adhesion, swarming and biofilm formation are much better understood (Parsek & Greenberg
2000, Ren et al. 2002, Qian et al. 2007).
Antibiotic activities of macroalga-associated bacteria
Antimicrobial activity is widespread among algaassociated bacteria. Wiese et al. (2009b) showed that
almost 50% of a total of 210 isolates of the epiphytic
bacterial community of Saccharina latissima (Baltic
Sea, Germany) inhibited the growth of at least one
microorganism from a panel covering Gram-negative
and Gram-positive bacteria. Burgess et al. (1999) demonstrated that 35% of the surface-associated bacteria
isolated from various macroalgae and invertebrates in
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Goecke et al.: Marine macroalgal–bacterial interactions
Table 4. Bioactive compounds produced by macroalgal associated bacteria. AF = antifungal activity, AP = antiprotozoal activity,
AS = antisettlement activity, GNI = antibiotic activity against Gram-negative bacteria, GPI = antibiotic activity against Grampositive bacteria, MG = morphogenesis activity, PH = photosynthetic compound
Compound
Chemical class
2, 4 dibromo-6chlorophenol
Halogenated
phenol
2, 4-diacetyl
phloroglucinol
Activity
Producing bacterium
Macroalgae
Source
GPI
Pseudoalteromonas
luteoviolacea
Padina australis
Jiang et al. (2001)
Phenol
GPI
Pseudomonas sp.
Ceratodyction
spongiosum
Isnansetyo et al.
(2001)
Chlorophyll d
Pyrrole
PH
Acaryochloris sp.
Ahnfeltiopsis
flabelliformis
Murakami et al.
(2004)
Cyclo-[isoleucylprolylleucyl-alanyl]
Tetrapeptide
GPI
Pseudoalteromonas
sp.
Digenea sp.
Rungprom et al.
(2008)
Cyclo-(L-prolylL-glycine)
Diketopiperazines
GPI
Pseudoalteromonas
luteoviolacea
Padina australis
Jiang et al. (2001)
Cyclo-(L-phenyl alanyl-4R)hydroxy-L-proline
Diketopiperazines
GPI
Pseudoalteromonas
luteoviolacea
Padina australis
Jiang et al. (2001)
Haliangicin
β-methoxyacrylate
AF
Haliangium luteum
Undetermined
algae
Fudou et al. (2001)
Korormicin
γ-lactone derivate
GNI
Pseudoalteromonas
sp. F-420
Halimeda sp.
Yoshikawa et al.
(1997)
Macrolactines G, M
Lactones
GPI
Pseudomonas sp.
Red algae
Gerard et al.
(1997)
Macrolactines G, M, A, F
Lactones
GPI
Bacillus sp.
PP19-H3
Schizymenia
dubyi
Nagao et al. (2001)
Massetolide A
Lipopeptide
GPI
Pseudomonas sp.
Red algae
Gerard et al.
(1997)
Pelagiomycin A
Phenazine
GPI,
GNI
Pelagiobacter
variabilis
Pocockiella
variegata
Imamura et al.
(1997)
–
Peptide
AS
Pseudoalteromonas
tunicata
Ulva lactuca
Egan et al. (2001b)
–
Peptide
AS
Alteromonas sp.
Ni1-LEM
Rhodymenia sp.
Silva-Aciares &
Riquelme (2008)
Protein 30, 7 kDa
Protein
GPI
Bacillus
licheniformis
Fucus serratus
Jamal et al. (2006)
Thallusin
Pyridine
MG
Cytophaga/
Flavobacterium/
Bacteroidetes group
Monostroma sp.
Matsuo et al.
(2003)
Violacein
Alkaloid
AP
Pseudoalteromonas
tunicata, P. ulvae
Ulva australis
Matz et al. (2008)
YP1
Tambjamine
AF
Pseudoalteromonas
tunicata
Ulva australis
Franks et al. (2006)
Scottish waters produced antimicrobial substances.
From a total of 280 strains isolated from 7 macroalgae,
21% showed antibacterial activity (Boyd et al. 1999b).
Of the isolates from 9 brown macroalgae, 20% were
antibiotically active as were 33% of the isolates from 9
red algae collected from Japanese waters of the Pacific
Ocean (Kanagasabhapathy et al. 2006, 2008). Penesyan et al. (2009) obtained 325 bacterial isolates from
the surface of Delisea pulchra and Ulva australis in
Australia and demonstrated antibiotic activity of 12%
of the strains. Microbulbifer sp. was the dominant biological active bacterium in this study.
Antimicrobial active isolates from all mentioned
macroalgae were phylogenetically assigned to diverse
genera comprising Pseudomonas, Pseudoalteromonas,
Stenotrophomonas, Vibrio, Aeromonas, Shewanella,
Streptomyces and Bacillus species (Wiese et al. 2009b).
Many Bacillus species are efficient producers of
antimicrobial compounds and therefore highly successful colonizers of macroalgal surfaces (Trischman et
al. 2004, Kanagasabhapathy et al. 2006). Most of the
isolates with high antifouling activity obtained by Burgess et al. (2003) were identified as Bacillus species,
i.e. B. pumilus, B. licheniformis and B. subtilis. Besides
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Mar Ecol Prog Ser 409: 267–300, 2010
Bacillus species, Pseudoalteromonas spp. are commonly found on marine macroalgae (Wang et al. 2008).
Many of them also produce biologically active molecules (Holmström et al. 1998, Kalinovskaya et al. 2004,
Skovhus et al. 2007). For example, 3 epiphytic strains
of Pseudoalteromonas sp. isolated from Ulva lactuca
were able to inhibit the growth of a variety of bacteria
and fungi (Egan et al. 2000, 2001a,b): P. tunicata was
able to prevent biofouling by growth inhibition of other
surface-associated microorganisms. For this purpose, it
produced at least 5 target-specific compounds (Holmström et al. 1992, James et al. 1996) (Table 4), including
a large antibacterial protein (James et al. 1996), a small
polar heat-stable anti-larval molecule (Holmström et
al. 1992), a putative antialgal peptide (Egan et al.
2001b), an antifungal alkaloid (Franks et al. 2006) and
also violacein, a purple pigment that inhibits protozoan
grazing (Matz et al. 2008). This chemical arsenal has
been shown to be important for the survival of P. tunicata in its highly competitive marine surface environment (Rao et al. 2005, 2007, Thomas et al. 2008, and
references therein). Production of a range of compounds active against a variety of target organisms is a
characteristic feature of these bacteria and may largely
promote their competition and colonization of algal
surfaces (Holmström & Kjelleberg 1999, Patel et al.
2003, Rao et al. 2005).
Bacteria producing antibiotic substances reflect an
important part of bacterial communities on surfaces of
marine organisms as compared to free-living bacterial
communities (Mearns-Spragg et al. 1998, Zheng et al.
2005, Kanagasabhapathy et al. 2008). However, we
still have a long way to go in understanding how bacteria really protect their hosts and what kind of compounds they may produce under the multifactorial natural conditions in situ (Bode et al. 2002). For example,
a marine actinomycete (SS-228) was shown to produce
an antibiotic compound only when the growth medium
was supplemented with Laminaria sp., a macroalgae
common in the habitat from which the strain was
obtained (Okazaki et al. 1975). Inhibitory activities
against other epiphytic bacteria are of great importance in microhabitats such as an algal surface, where
competition for an attachment site is frequent (Lemos
et al. 1985, Mearns-Spragg et al. 1998, Yan et al. 2002,
Rao et al. 2007).
Chemical defense of macroalgae against
microorganisms
The defending interaction of macroalgae with
biofilms is well documented and the surfaces of many
macroalgae remain relatively free of epibiosis. However, few studies have investigated if secondary
metabolites are released from macroalgae and affect
planktonic bacteria directly (Nylund & Pavia 2005,
Paul et al. 2006, Dubber & Harder 2008, Lam et al.
2008a). Lu et al. (2008) showed that macroalgae like
Ulva clathrata have an inhibitory effect on Vibrio
anguillarum, a fish and mussel pathogen, although not
reducing the total amount of heterotrophic bacteria.
This effect was explained by some unknown chemical
substances, either released from U. clathrata or produced by the alga-associated microorganisms. Recently,
Pang et al. (2006a) observed that in polycultures with
the red macroalga Gracilaria textorii the total number of Vibrio species (V. alginolyticus and V. logei )
was controlled. Even more, after inoculation of V.
parahaemolyticus into cultures of the red macroalga
Grateloupia turuturu, the bacterium was inhibited in
its growth and finally disappeared from the cultures
(Pang et al. 2006b).
Antibiotic activities of macroalgal extracts and
metabolites
Given that algae lack cell-based immune responses
and are continuously exposed to a broad array of
potentially deleterious microorganisms, it is reasonable to hypothesize that the production of bioactive
secondary metabolites acts as a fundamental mechanism of antimicrobial defense to deter microbial attack
(Engel et al. 2002). Macroalgae may secrete antifouling compounds into the surrounding seawater
and retain antigrazing compounds within the thallus
structure (Armstrong et al. 2001). The production of
inhibitory substances from macroalgae was noted as
early as in 1917 (Ara 2001) and since then the antibacterial activity of extracts of macroalgae has been
described in many studies around the world (Yan et al.
2003, Bhakuni & Rawat 2005, Puglisi et al. 2007, Dubber & Harder 2008, and literature therein) (Table 5).
Many different compounds produced by macroalgae
exhibit antibiotic activity, for example fatty acids, phenols, acetylenes, various terpenes, coumarins, carbonyls, and polysaccharides (Bhakuni & Silva 1974,
Hoppe et al. 1979 and literature therein, Ballantine et
al. 1987, Lustigman et al. 1992, Lobban & Harrison
1996, Steinberg et al. 1997, Potin et al. 1999, Ara 2001,
Sandsdalen et al. 2003; Table 5). These biological
activities might have a protective function by elimination or control of the number of pathogens, epiphytes
or endophytes (Hornsey & Hide 1976b, Hoppe et al.
1979, Smit 2004, Plouguerne et al. 2008).
While a large proportion of the literature deals with
antimicrobial activities of marine macroalgal extracts
and secondary metabolites (Table 5), little is known
about how these compounds act in an ecological con-
279
Goecke et al.: Marine macroalgal–bacterial interactions
Table 5. Examples of antimicrobial and antifouling compounds isolated from macroalgae. AV = antiviral, AE = antifouling, AF =
antifungal activity, GNI = antibiotic activity against Gram-negative bacteria, GPI = antibiotic activity against Gram-positive
bacteria
Macroalga
Compounds
Chlorophyta
Avrainvillea nigricans
Caulerpa spp.
Codium iyengarii
Penicillus capitatus
Tydemania expeditionis
Ulva fasciata
5’-hydroxy isoavrainvilleol
Sesquiterpenoids
Iyengaroside-A, clerosterol galactoside
Capisterones A, B
Sulphated triterpenoids
Labdane diterpenoids
GPI
GPI, GNI
GPI, GNI
AF
AF
GNI
Colon et al. (1987)
Paul et al. (1987)
Ali et al. (2002)
Puglisi et al. (2004)
Jiang et al. (2008)
Chakraborty et al. (2010)
Heterokontophyta, Phaeophyceae
Canistrocarpus cervicornis
Cystoseira spinosa var. squarrosa
Cystoseira tamariscifolia
Dictyotaceae
Dictyopteris zonarioides
Dictyota menstrualis
Dilophus guineensis
Dilophus okamurai
Fucus vesiculosus
Landsburgia quercifolia
Lobophora variegata
Sargassum spp.
Stoechospermum marginatum
Stoechospermum marginatum
Diterpenes
Tetraprenyltoluquinol
Methoxybifurcarenone
Dolabellane derivatives
Zonarol & isozonarol
Dictyol D, pachydictyol A
Dilophic acid
Spatane-type diterpenes
Polyhydroxylated fucophlorethol
1, 4-naphthoquinone
Lobophorolide
Polyphenols
Spatane diterpenoids
Sulfated fucan
AE
GPI, GNI
GNI
AF
AF
AE
GPI
AE
GPI, GNI
GPI, AF
AF
AE, GNI
GPI
AV
Bianco et al. (2009)
Amico et al. (1988)
Bennamara et al. (1999)
Tringali et al. (1986)
Fenical et al. (1973)
Schmitt et al. (1995)
Schlenk & Gerwick (1987)
Kurata et al. (1988)
Sandsdalen et al. (2003)
Perry et al. (1991)
Kubanek et al. (2003)
Sieburth & Conover (1965)
De Silva et al. (1982)
Adhikari et al. (2006)
Halomethanes, haloether, haloacetales
Poly-brominated 2- heptanone
Bromophycolides
P-hydroxybenzaldehyde
Almazole D
Halogenated furanones
Halogenated furanones
Galactan sulphate
3-hydroxi-4-methyl acetophenone
Brominated sesquiterpenes
Pannosanol, pannosane
Laurinterol, isolaurinterol
Brominated sesquiterpenes
Lanosol ethyl ether
Bromophenols
Bromosphaerone,
12S-hydroxybromosphaerodiol
GPI, GNI
GNI
AF
GPI, GNI
GNI
AE
GPI, GNI
AV
GPI, GNI
GPI, GNI
GNI
GNI
GPI, GNI
GPI, GNI, AF
GPI, GNI
GPI
Paul et al. (2006)
Nylund et al. (2008)
Lane et al. (2009
Fenical & McConnell (1976)
N’Diaye et al. (1996)
Maximilien et al. (1998)
Wright et al. (2006)
Chattopadhyay et al. (2007)
Valdebenito et al. (1982)
Vairappan et al. (2010)
Suzuki et al. (2001a)
Vairappan et al. (2001b)
Bansemir et al. (2004)
Barreto & Meyer (2006)
Xu et al. (2003)
Etahiri et al. (2001)
Rhodophyta
Asparagopsis armata
Bonnemaisonia hamifera
Callophycus serratus
Dasya pedicellata var. stanfordiana
Delesseriaceae
Delisea pulchra
Delisea pulchra
Grateloupia indica
Laurencia chilensis
Laurencia majuscula
Laurencia pannosa
Laurencia spp.
Laurencia spp.
Osmundaria serrata
Rhodomela confervoides
Sphaerococcus coronopifolius
text (Engel et al. 2002). Engel et al. (2006) explored the
antimicrobial effects of extracts from several marine
macroalgae against algal saprophytes, parasites, and
pathogens. It was concluded that the antimicrobial
metabolites selectively target marine microorganisms,
although the susceptibility of ecologically relevant
bacteria has rarely been studied (Yoshikawa et al.
1997, Puglisi et al. 2007, Kanagasabhapathy et al. 2008).
From an ecological perspective, antimicrobial defense mechanisms of marine macroalgae may reduce
epibiosis, inhibit premature decomposition and directly
provide resistance to infectious diseases (Engel et al.
2006). The required defense substances may be expressed constitutively or may be induced in response
Activity
Source
to contact with the target organisms and their chemical
signals, respectively (Cronin & Hay 1996, Amsler &
Fairhead 2005). The inducible defense allows metabolic cost savings and is advantageous due to a lower
risk of autotoxicity and resistance adaptation (Macaya
et al. 2005, Medeiros et al. 2007, Macaya & Thiel 2008).
An increasing number of studies is related to the induced defense mechanisms of macroalgae against
herbivores. Research on the induced defense mechanisms against microbial pathogens or epibiosis is still
limited. Recently, Vairappan et al. (2010) were the first
to demonstrate the highly selective antibiotic activity
of extracts from the epiphytic macroalga Laurencia
majuscula against 6 algal pathogenic bacteria. They
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Mar Ecol Prog Ser 409: 267–300, 2010
were able to identify 4 halogenated compounds whose
concentration increased more than 120% during an
ice-ice disease outbreak in the host basibiont, the
macroalga Kappaphycus alvarezii (Table 5). Interestingly, in another species of these red macroalgae,
Laurencia obtusa, the dynamics of vesicle transport
from corps en cerise (specific structures where those
macroalgae accumulate these halogenated secondary
metabolites) and their eventual exocytosis were shown
to be induced in relation to bacterial biofilms (Paradas
et al. 2010). The authors suggested a direct correlation
with this process and the inhibition of microfouling on
the macroalgal surface.
Oxidative burst—an antibacterial response of
macroalgae
In addition to the production of antibiotic compounds, macroalgae are able to use oxidative burst as
a defense mechanism as described for higher plants
(Weinberger et al. 1999, 2002, Dring 2005, Ar Gall et al.
2008). This process is a non-specific defense response
against surface colonization typically characterized by
a rapid activation of reactive oxygen species causing
death of the pathogen (Bouarab et al. 1999, Weinberger & Friedlander 2000a,b, Steinberg & de Nys
2002, Potin 2008). The oxidative burst is triggered by
cell-cell recognition, involving the perception of signal
molecules or cell wall compounds from the invading
organism by the algal cell membrane (Küpper et al.
2006). Common elicitors of non-specific host responses
are oligosaccharides, glycoproteins, and glycopeptides
(Küpper et al. 2001). Recently, other compounds such
as methyl jasmonate and free fatty acids (in particular
arachidonic and linolenic acid) were also found to be
strong triggers of an oxidative burst in Laminaria digitata (Küpper et al. 2009). In particular, the elicitation of
defense mechanisms by oligosaccharides has been
studied in macroalgae (e.g. Potin et al. 1999, Ar Gall et
al. 2008). This involves the degradation of the host cellwall polysaccharides by enzymes released from various pathogens, comprising epiphytic bacteria (Weinberger et al. 1999, Weinberger & Friedlander 2000a,b,
Küpper et al. 2002) and algal endophytes (Bouarab et
al. 1999, Küpper et al. 2002). This was shown for the
brown alga L. digitata, where oligosaccharides derived
from alginate elicit a distinct oxidative burst in the cortical cells of sporophytes and thereby control the populations of epiphytic bacteria (Küpper et al. 2001).
Küpper et al. (2002) investigated 45 species of brown
algae with regard to their ability to respond to oligoalginates with an oxidative burst. They found that a
total of 15 macroalgal species reacted, all of them
belonging to an alginate-rich group with complex thal-
lus morphology. But there is also evidence for a constitutive release of hydrogen peroxide in red macroalgae
e.g. Solieria chordalis, as a mechanism to prevent both
the establishment of bacterial biofilms and the subsequent development of algal epiphytes (Ar Gall et al.
2008). In addition to algal elicitors, Küpper et al. (2006)
demonstrated that components of the outer membranes of Gram-negative bacteria may be considered
as exogenous elicitors in brown macroalgae. In the red
agarophyte Gracilaria conferta bacterial elicitors are
presumably represented by a low-molecular weight
peptide (Weinberger & Friedlander 2000a).
These results demonstrate that defense pathways
exist in marine macroalgae which are similar to those
known from animals and land plants (Bouarab et al.
2004, Weinberger 2007). Interestingly, the oxidative
burst is known to direct a variety of secondary defense
responses like the generation and release of volatile
halogenated compounds and the peroxidation of fatty
acids (Küpper et al. 2001, 2006, Weinberger et al. 2002,
Cosse et al. 2007, Potin 2008). Induction of the oxidative burst within red and brown macroalgae is followed by a rapid increase in emission of iodine-containing halocarbons, molecular iodine, and also in the
brominating activity (Weinberger et al. 1999, Palmer et
al. 2005).
Quorum sensing and its role in bacterial–macroalgal
interactions
Quorum sensing (QS) is a cell to cell communication
mechanism that allows bacteria to coordinate swarming, biofilm formation, stress resistance, and production of secondary metabolites in response to an excess
of the threshold of QS signals (Paul & Ritson-Williams
2008, Dobretsov et al. 2009). Gram-negative bacteria,
such as Pseudomonas or Vibrio strains, produce N-acyl
homoserine lactones (AHLs) as signalling compounds.
Pseudomonas spp. are also known to produce diketopiperazines acting as QS signals (Dickschat 2010).
The signal molecules γ-butyrolactones and oligopeptides are known to be synthesized by Gram-positive
bacteria, e.g. members of the genera Streptomyces or
Bacillus (reviewed by Dobretsov et al. 2009).
The interaction between zoospores of eukaryotic
green macroalgae (Ulvales) with Vibrio anguillarum
indicates algal susceptibility to quorum sensing AHL
molecules (Joint et al. 2002, Wheeler et al. 2006).
Although the specific mechanism regulating these
responses to AHLs is not known, it was shown that the
AHL molecules affect the calcium influx into the spores
of Ulva sp., affecting their motility towards the surfaces
where they eventually settle (Diggle et al. 2007, Joint
et al. 2007). In addition, it has been demonstrated that
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Goecke et al.: Marine macroalgal–bacterial interactions
life cycle completion and spore release in the red epiphytic alga Acrochaetium sp. strongly depend on
AHLs, which are produced by bacteria associated with
the algal basibiont Gracilaria chilensis (Weinberger et
al. 2007). These findings of AHL perception in green
and red algae confirm that AHL signalling is more
widespread among eukaryotes than previously thought.
This indicates a more general importance of the associated microbial communities in interactions with macroalgae. As we mentioned before, bacterial biofilms play
an important role in the development of macroalgal
communities. Hence, the ability to exploit a bacterial
sensory system makes an important contribution to the
ecological success of macroalgae (Tait et al. 2005, Joint
et al. 2007).
Algae reduce harmful effects by controlling bacterial
colonization by interfering with the bacterial QS systems, which regulate several bacterial traits related to
colonization (Gram et al. 1996, Steinberg et al. 1997,
Dworjanyn et al.1999). During the past decade it has
been shown that various macroalgae are able to stimulate, inhibit or inactivate QS signals in bacteria by producing QS inhibitors or analogues thereof (Maximilien
et al. 1998, Joint et al. 2007, Kanagasabhapathy et al.
2009, Table 6). The Australian red macroalga Delisea
pulchra produces halogenated furanones, structural
analogues to N-acyl homoserine lactones. These furanones protect the algal surfaces by interfering with
AHL-regulated processes and selectively inhibit bacterial colonization and biofilm formation (Maximilien et
al. 1998, Rasmussen et al. 2000, Manefield et al. 2002).
In addition to the furanones of D. pulchra, a variety of
bacteria and eukaryotes have been shown to produce
cyclic dipeptides that can act as AHL mimics and affect
QS-regulated behaviour in other bacteria (Dobretsov
et al. 2009, Dickschat 2010). Recently, Kanagasabhapathy et al. (2009) suggested that certain epibiotic bacteria from the brown macroalgae Colpomenia sinuosa
may play a role in defense mechanisms and suppress
the settlement of other competitive bacteria by producing quorum sensing inhibitors (QSI) or QSI-like compounds. AHL-antagonists and inhibitors of the AHL
regulatory system lead to an inhibition of bacterial colonization in an entirely different way from antibiotic
substances (Givskov et al. 1996, Manefield et al. 1999,
2002). Their action results in lower bacterial abundance on the algal surface relative to other surfaces
that are not controlled by such or similar mechanisms
(Maximilien et al. 1998, Steinberg & de Nys 2002).
BIOSYNTHETIC ORIGIN OF BIOLOGICALLY
ACTIVE METABOLITES
Macroalgae are prolific natural product synthesizers.
Until now, approximately 2000 secondary metabolites
have been isolated from these algae, most of them
displaying biological activities (Medeiros et al. 2007).
Nevertheless, marine microorganisms have also been
shown to be an important source for novel natural
products (Fenical 1993, Penesyan et al. 2010). Considering that so far virtually all macroorganisms collected
and extracted for chemical studies include the associated microorganisms, questions about the true biosyn-
Table 6. Quorum sensing (QS) inhibitors observed in algae (modified from Dobretsov et al. 2009). AHL = N-acyl homoserine lactones
Algae
Compound
Activity
Source
MICROALGAE
Chlorophyta
Chlamydomonas reinhardtii
Lumichrome
Mimic AHL signals
Rajamani et al. (2008),
Teplitski et al. (2004)
MACROALGAE
Chlorophyta
Caulerpa sp.
Not identified (algal extract)
AHL inhibitors
Skindersoe et al. (2008)
Heterokontophyta, Phaeophyceae
Laminaria digitata
Hypobromous acid
Rhodophyta
Ahnfeltiopsis flabelliformis
Deactivates AHL by
Borchardt et al. (2001)
interfering with QS genes
Betonicine, floridoside
and isethionic acid
Compete with AHL signals Kim et al. (2007)
Delisea pulchra
Halogenated furanones
Mimic AHL signals,
inhibit gene expression
Manefield et al. (1999)
Galaxauraceae
Not identified (algal extract)
AHL inhibitors
Skindersoe et al. (2008)
Laurencia sp.
Not identified (algal extract)
AHL inhibitors
Skindersoe et al. (2008)
Unidentified red algae
Not identified (algal extract)
AHL inhibitors
Skindersoe et al. (2008)
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Mar Ecol Prog Ser 409: 267–300, 2010
thetic origin of molecules isolated from macroalgae
need to be addressed. In several cases, it has already
been proven that metabolites initially assigned to the
basibionts are in fact of microbial origin (Jensen &
Fenical 1994, Schmidt 2005, Dobretsov et al. 2006a,
König et al. 2006, Egan et al. 2008, Jones et al. 2008,
Lane & Kubanek 2008, Rungprom et al. 2008). Chlorophyll d, for example, is not a constituent of red algae as
was described for more than 60 yr. In fact, it does not
even occur in eukaryotes at all, but is produced by the
cyanobacterium Acaryochloris spp. (Murakami et al.
2004, Larkum & Kühl 2005; Table 4). Further studies
like this including labelling experiments and genetic
studies of biosynthetic genes will reveal the producing
part of the association for other macroalga-epibiontsystems.
strategies have to be developed to prevent infection of
macroalgae by such pathogens.
On the other hand, there is an increasing interest in
algae-associated microorganisms as a source for natural bioactive substances (Egan et al. 2008). Algaassociated bacteria represent an important potential
source of new substances and have been identified as
a promising source of new bioactive and antimicrobial
metabolites (Yan et al. 2002, Penesyan et al. 2009).
Novel infectious diseases of humans, reemerging diseases, and the widespread distribution of multidrugresistant pathogenic bacteria clearly indicate a strong
need to develop new antibiotics (Fenical 1993, Skindersoe et al. 2008). Table 4 provides a comprehensive
overview of compounds produced by macroalgaassociated bacteria. Most of these compounds including peptides or diketopiperazines were produced by
members of Pseudoalteromonas.
APPLIED ASPECTS OF
BACTERIAL–MACROALGAL INTERACTIONS
CONCLUSIONS AND PERSPECTIVES
The development and expansion of macroalgal farming stresses the need for understanding the relationship between macroalgae and symbiotic as well as
pathogenic microorganisms in both wild and cultivated populations (Correa 1996). The extensive farming of brown, red and green macroalgae in Asia has
shown that all are susceptible to disease (Craigie &
Correa 1996). In aquaculture, secondary bacterial
infections contribute to disintegration of the infected
tissue, finally leading to thallus rupture, breaking-off
of macroalgae from culture lines and massive biomass
loss (Vairappan et al. 2001a, 2008). Infectious diseases
in macroalgae might be highly destructive as in the
case of the green spot rot of Undaria spp. and the white
rot in Nereocystis spp. (Lavilla-Pitogo 1992, Correa et
al. 1993, Park et al. 2006, and references therein). Red
rot disease is caused by the fungal pathogen Phytium
porphyrae affecting different Porphyra species, one of
the most popular edible and extensively cultivated
macroalga, especially in Asia. In Japan, the disease
causes losses of about 40 to 60 million US$ every year
(Woo et al. 2002). Despite some knowledge of the
pathogens and diagnosis of the diseases, little is
known concerning the ecology of microbial pathogens
of these macroalgae (Andrews 1976, Jaffray & Coyne
1996, Correa 1997; Table 3). The growing use of
macroalgae and their products enforces the need to
understand the nature and severity of diseases that can
be anticipated in macroalgal mariculture (Apt 1984).
The development of appropriate strategies will provide
adequate and improved protection of the macroalgae
in order to lower commercial risks (Park et al. 2006).
For this purpose, pathogens of macroalgae have to be
identified and characterized at the species level and
Epibiotic bacteria are fast colonizers, highly adaptative and capable of rapid metabolization of algal exudates, and therefore play a key role in the colonization
and biofouling process on macroalgae (Lachnit et al.
2009). Chemical interactions between different species
of bacteria affect the production and secretion of secondary metabolites in these microorganisms (Jensen &
Fenical 1994, Burgess et al. 1999, Rao et al. 2005). The
competition for space between epibiotic bacteria based
on compounds may provide an antifouling protection
to the algal basibiont (Armstrong et al. 2001, Rungprom et al. 2008). Since symbiotic bacteria, pathogens,
and foulers first select, then settle, and finally attach to
the host, macroalgae may prevent damage by also producing secondary metabolites that inhibit one or all of
these steps. Such metabolites represent the chemical
first line of defense against microbial challenge. If the
bacterial attachment is not stopped successfully, other
secondary metabolites may inhibit the growth, survival, virulence, or reproduction of possibly invading
organisms. These second line compounds may be produced by the macroalgae or by epiphytic and endophytic microbes associated with them (Egan et
al. 2000, Than et al. 2004, Rao et al. 2007, Lane &
Kubanek 2008). A mutualistic relationship can be postulated in which the bacterial community protects the
host from biofouling, while the host surface may provide nutrients and physical protection to the bacteria
(Penesyan et al. 2010). The selection of these ‘symbiotic’ microorganisms might also be chemically mediated (Lachnit et al. 2010). However, after more than
20 yr of research on this topic, there is still no experimental evidence demonstrating if or how host organ-
Goecke et al.: Marine macroalgal–bacterial interactions
isms selectively attract and harbor such epibionts
(Harder 2009). There is an enormous variety of different metabolites as possible mediators of interspecies
interactions in the algal biosphere, including products
of the algal host, pathogens, foulers, and symbionts.
Although bacterial secondary metabolites are likely to
participate in such interactions, little is known about
the role of bacterial secondary metabolites in mediating such ecological interactions (Maximilien et al.
1998, Meusnier et al. 2001). An interesting aspect is the
chemical interaction between hosts and their symbionts, the details, including host specificity, nutrients
and metabolite exchange, and cell–cell communication have to be revealed by further studies.
In order to develop a better understanding of chemically mediated communication on and with the alga, it
is important to detect the allocation of secondary
metabolites within the host tissues (Dworjanyn et al.
1999, 2006, Sudatti et al. 2008). For such investigations,
it is essential to measure the in situ concentrations and
the methods of release of putative deterrents (Krug et
al. 2006, Paradas et al. 2010). Only a few analyses have
attempted to measure the concentration of these compounds in seawater and host tissues (de Nys et al. 1998,
Maximilien et al. 1998, Dworjanyn et al. 1999, Manefield et al. 1999, Kubanek et al. 2003, Paul et al. 2006,
Sudatti et al. 2006). The recent improvement of techniques for detecting natural products on tissue surfaces, such as desorption electrospray ionization mass
spectrometry (DESI-MS), will provide new sensitive
and effective approaches to resolve localization and
origin of these compounds (Lane et al. 2009, Nyadong
et al. 2009). Improved chemical and molecular biological methods coupled with ecologically relevant bioassays are likely to lead to new discoveries (Hay 2009)
and to a better understanding of the development of
complex chemical defense mechanisms against microbial threats. The results will enforce our knowledge of
distinct functions of bacteria in various kinds of interactions between macroalgae and bacteria, as well as
within the bacterial community.
In addition to the chemical point of view, we also
need more detailed studies of the bacterial communities and their development, using new molecular
approaches. Until now, most investigations have
focussed on 1 or 2 different techniques to describe
communities. From our point of view, a synopsis between culture-dependent and -independent methods
is needed. Various authors have already shown that
the diversity of a given bacterial community cannot be
described by applying either genetic or culture-based
methods (Jensen et al. 1996, Tujula et al. 2006, Longford et al. 2007, Penesyan et al. 2009). Since most studies presented qualitative information but did not analyze abundances and ratios that occur in situ, the
283
application of quantitative or semi-quantitative methods is required, such as cloning techniques, cytogenetic fluorescence in situ hybridization (CFISH), real
time quantitative PCR (qPCR), denaturing gradient gel
electrophoresis (DGGE), and terminal restriction fragment length polymorphism of DNA (T-RLFP), as well
as metagenome studies. The genes used for these
investigations should comprise phylogenetic markers
as well as functional genes in order to obtain insight
into biosynthetic pathways and their regulation, in particular of those used in the production of the interacting small molecules. Community description should be
extended by studying the geographic distribution
among different host populations with respect to the
associated bacterial communities, which are necessary
to clarify eventual effects (Wright et al. 2000).
To sum up, there is a strong need to integrate aspects
of ecology, cell biology, and chemistry in further studies (Steinberg & de Nys 2002) in order to understand
the production and the distribution of the bioactive
molecules in situ as well as their ecological impact on
the macroalgal–bacterial interactions.
Acknowledgements. This study was financed by the DAAD
(German Academical Exchange Service), the CONICYT
(Comité Nacional de Ciencia y Tecnología, Chile), and the
Ministry of Science, Economic Affairs and Transport of the
State of Schleswig-Holstein (Germany) within the frame of
‘Future Program of Economy’, which is supported by the
European fund for regional development (EFRE).
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Appendix 1. Studies of bacterial communities attached to the surface of different macroalgae over the last 40 yr. CUD = culture
dependent methods. Microscopical methods: EPF = epifluorescence microscopy, EM = electron microscopy, SEM = scanning
electron microscopy, STE = stereoscopic microscopy, TEM = transmission electron microscopy. Molecular techniques: CLO =
cloning, CFISH = cytogenetic fluorescence in situ hybridization, DGGE = denaturing gradient gel electrophoresis, FISH = fluorescence in situ hybridization, IFN = immunofluorescent detection, RQT = real time quantitative PCR, RFLP = restriction fragment
length polymorphism, TRFLP = terminal restriction fragment length polymorphism of DNA
Macroalga
Chlorophyta
Chlorophyta spp.
Caulerpa cupressiodes
Caulerpa mexicana
Caulerpa prolifera
Methodology
Location
Source
STE
DGGE, SEM
DGGE, SEM
DGGE, SEM
EM, STE
San Juan Island, USA
Tampa Bay, USA
Tampa Bay, USA
Tampa Bay, USA
Tampa Bay, USA
Bland & Brock (1973)
Delbridge et al. (2004)
Delbridge et al. (2004)
Delbridge et al. (2004)
Dawes & Lohr (1978)
Goecke et al.: Marine macroalgal–bacterial interactions
297
Appendix 1 (continued)
Macroalga
Methodology
Location
Source
Caulerpa racemosa
Caulerpa sertulariodes
Caulerpa taxifolia
TRFLP, SEM
DGGE, SEM
RFLP
Dobretsov et al. (2006b)
Delbridge et al. (2004)
Chaetomorpha brachygona
Chaetomorpha media
Chaetomorpha sp.
CUD
CUD
CUD
Hong Kong
Tampa Bay, USA
Mediterranean, Tahiti,
Philippines, Australia
Tolo, Hong Kong
Anjuna & Baga, India
Vellar Estuary, India
Chara aspera
Cladophora rupestris
Codium cylindricum
Codium fragile
Enteromorpha compressa
Enteromorpha intestinalis
Enteromorpha linza
Enteromorpha sp.
FISH
CUD
CUD
CUD
CUD
CUD
CUD
CUD
Baltic Sea, Germany
France
Tolo, Hong Kong
Scotland
Ria de Arosa & Pontevedra, Spain
Ria de Arosa & Pontevedra, Spain
Japan
Vellar Estuary, India
IFN
CUD, EPF
SEM, EM
CUD
CUD
SEM, EM
DGGE, CLO
DGGE,CFISH
DGGE, CLO
CUD, EPF
CUD
DGGE
TRFLP
CUD
CUD
CUD
CUD
CUD, TEM
CUD, TEM
RTQ, DGGE
CFISH, DGGE
CUD, SEM
CUD
CUD, SEM
CUD, SEM
CUD
CUD
CUD
RTQ, DGGE
CUD, EPF
RTQ, DGGE
Auckland, New Zealand
Bahamas Islands
Lecce, Italy
Japan
Puerto Deseado, Argentina
Sardinia, Italy
Shark Point, Australia
Shark Point, Australia
Sydney, Australia
Sydney, Australia
Sydney, Australia
Baltic & North Sea, Germany
Chañaral, Chile
Anjuna & Baga, India
Scotland
Tolo, Hong Kong
Spain
Massachusetts, USA
Sydney, Australia
Kattegat, Denmark
Shark Point, Australia
Jiaozhou, China
Tuandao Bay, China
Malaysia
Hong Kong
Las Salinas Beach, Spain
Pleubian, France
Japan
Kattegat, Denmark
Uminokoven, Japan
Kattegat, Denmark
Meusnier et al. (2001)
Kong & Chan (1979)
Ramaiah & Chandramohan (1992)
Lakshmanaperumalsamy &
Purushothaman (1982)
Hempel et al. (2008)
Barbeyron & Berger (1989)
Kong & Chan (1979)
Boyd et al. (1999a,b)
Lemos et al. (1985)
Lemos et al. (1985)
Shiba & Taga (1980)
Lakshmanaperumalsamy &
Purushothaman (1982)
Booth & Hoppe (1985)
Jensen et al. (1996)
Colombo (1978)
Shiba & Taga (1980)
Gallardo et al. (2004)
Colombo (1978)
Longford et al. (2007)
Tujula et al. (2010)
Burke et al. (2009), Delbridge et al. (2004)
Rao et al. (2006, 2007)
Penesyan et al. (2009)
Lachnit et al. (2009)
Moran et al. (2008)
Ramaiah & Chandramohan (1992)
Boyd et al. (1999a,b)
Kong & Chan (1979)
Lemos et al. (1985)
Waite & Mitchell (1976)
Egan et al. (2000)
Skovhus et al. (2004)
Tujula et al. (2006, 2010)
Duan et al. (1995)
Wang et al. (2009)
Vairappan & Suzuki (2000)
Dobretsov & Qian (2002)
Bolinches et al. (1988)
Liot et al. (1993)
Shiba & Taga (1980)
Skovhus et al. (2004)
Uchida & Murata (2004)
Skovhus et al. (2004)
Trondheimsfjord, Norway
Massachusetts, USA
Camp Varnum, RI, USA
Sea of Japan, Russia
Awaji Island, Japan
San Sebastian, Spain
Sea of Japan, Russia
Gijon, Spain
Awaji Island, Japan
Kommetjie, South Africa
Sieburth & Jensen (1967)
Cundell et al. (1977)
Sieburth & Tootle (1981)
Beleneva & Zhukova (2006)
Kanagasabhapathy et al. (2006, 2009)
Genilloud et al. (1994)
Beleneva & Zhukova (2006)
Genilloud et al. (1994)
Kanagasabhapathy et al. (2006)
Koop et al. (1982)
Halimeda copiosa
Halimeda tuna
Monostroma nitidum
Monostroma undulatum
Udotea petiolata
Ulva australis
Ulva compressa
Ulva fasciata
Ulva lactuca
Ulva pertusa
Ulva reticulata
Ulva rigida
Ulva sp.
Ulva spp.
Ulvaria fusca
Heterokontophyta, Phaeophyceae
Ascophyllum nodosum
CUD
SEM
SEM
Chordaria flagelliphormis
CUD
Colpomenia sinuosa
CUD
Cystoseira sp.
CUD
Desmarestia viridis
CUD
Dictyota dichotoma
CUD
Ecklonia cava
CUD
SEM
298
Mar Ecol Prog Ser 409: 267–300, 2010
Appendix 1 (continued)
Macroalga
Methodology
Location
Source
Ecklonia maxima
Ectocarpus siliculosus
Eisenia bicyclis
CUD
CUD
CUD
CUD, SEM
CUD
CUD
DGGE
EPF, CUD
SEM
CUD
CUD
IFN
DGGE
CUD
CUD
CUD, SEM
CUD
CUD
DGGE, EPF
CUD, SEM
CUD
CUD
CUD
CUD
CUD
CUD
DGGE
DGGE, CLO
CUD, EPF
SEM
SEM
CUD
CUD
CUD
CUD
IFN
IFN
CUD
CUD
CUD
CUD
CUD
CFISH
CUD
CUD
CUD
CUD
CUD
CUD
Oudekraal, South Africa
Tolo, Hong Kong
Japan
Japan
Spain
Scotland
Baltic & North Sea, Germany
White Sea, Russia
Camp Varnum, RI, USA
Gijon, Spain
Las Salinas Beach, Spain
Baltic Sea, Germany
Baltic & North Sea, Germany
Scotland
Gijon, Spain
Bay of Brest, France
Scotland
Roscoff, France
Bergen, Norway
Jiaozhou, China
Primor’e, Russia
Shandong Province, China
Sea of Japan, Russia
Tuandao Bay, China
Nova Scotia, Canada
Oudekraal, South Africa
Baltic & North Sea, Germany
Baltic & North Sea, Germany
Bahamas Islands
Bamfield Inlet, Canada
Bamfield Inlet, Canada
Awaji Island, Japan
Anjuna & Baga, India
Spain
Awaji Island, Japan
Auckland, New Zealand
Baltic Sea, Germany
Anjuna & Baga, India
Awaji Island, Japan
Awaji Island, Japan
Tolo, Hong Kong
Japan
Shark Point, Australia
Awaji Island, Japan
Sao Paulo, Brazil
Awaji Island, Japan
Awaji Island, Japan
Wando, Korea
Korea
Mazure & Field (1980)
Kong & Chan (1979)
Shiba et al. (1979)
Sakami & Sugiyama (1994)
Lemos et al. (1985)
Boyd et al. (1999a,b)
Lachnit et al. (2009)
Semenova et al. (2009)
Sieburth & Tootle (1981)
Genilloud et al. (1994)
Bolinches et al. (1988)
Booth & Hoppe (1985)
Lachnit et al. (2009)
Boyd et al. (1999a,b)
Genilloud et al. (1994)
Corre & Prieur (1990)
Boyd et al. (1999a,b)
Salaün et al. (2010)
Bengtsson et al. (2010)
Duan et al. (1995)
Dimitrieva & Dimitriev (1996)
Wang et al. (2008)
Beleneva & Zhukova (2006)
Wang et al. (2009)
Laycock (1974)
Mazure & Field (1980)
Lachnit et al. (2009)
Staufenberger et al. (2008)
Jensen et al. (1996)
Roland (1975)
Roland (1975)
Kanagasabhapathy et al. (2006)
Ramaiah & Chandramohan (1992)
Lemos et al. (1985)
Kanagasabhapathy et al. (2006)
Booth & Hoppe (1985)
Booth & Hoppe (1985)
Ramaiah & Chandramohan (1992)
Kanagasabhapathy et al. (2006)
Kanagasabhapathy et al. (2006)
Kong & Chan (1979)
Shiba & Taga (1980)
Tujula et al. (2006)
Kanagasabhapathy et al. (2006)
Menezes et al. (in press)
Kanagasabhapathy et al. (2006)
Kanagasabhapathy et al. (2006)
Kim et al. (2008)
Lee et al. (2006)
CFISH
CUD
TRFLP, EPF
CUD
CUD
IFN
CUD
SEM
CUD
Shark Point, Australia
France
Skagerrak, Sweden
Sea of Japan, Russia
Awaji Island, Japan
Baltic Sea, Germany
Skagerrak, Sweden
Camp Varnum, RI, USA
Gijon & Vigo, Spain
Tujula et al. (2006)
Barbeyron & Berger (1989)
Nylund et al. (2010)
Beleneva & Zhukova (2006)
Kanagasabhapathy et al. (2008)
Booth & Hoppe (1985)
Nylund et al. (2008)
Sieburth & Tootle (1981)
Genilloud et al. (1994)
Fucus ceranoides
Fucus serratus
Fucus sp.
Fucus vesiculosus
Himanthalia elongata
Laminaria digitata
Laminaria hyperborea
Laminaria japonica
Laminaria longicruris
Laminaria pallida
Laminaria saccharina
Lobophora variegata
Macrocystis integrifolia
Nereocystis luetkeana
Padina arborescens
Padina tetrastromatica
Pelvetia canaliculata
Petalonia fascia
Pilayella littoralis
Sargassum cinereum
Sargassum filicinum
Sargassum fusiformis
Sargassum hemiphyllum
Sargassum horneri
Sargassum linearifolium
Sargassum seratifolium
Sargassum sp.
Scytosiphon lomentaria
Undaria pinnatifida
Rhodophyta
Amphiroa anceps
Antithamnion plumula
Bonnemaisonia asparagoides
Camphylaephora hyphaeoides
Ceramium kondoi
Ceramium rubrum
Ceramium virgatum
Chondrus crispus
Goecke et al.: Marine macroalgal–bacterial interactions
299
Appendix 1 (continued)
Macroalga
Methodology
Location
Source
Chondrus oncellatus
Clathromorphum sp.
CUD
STE
SEM, CUD
CUD, DGGE
CUD
CFISH
DGGE
DGGE, CLO
DGGE, CLO
CUD
CFISH
CUD
IFN
CUD
CUD
CUD
CUD
CUD
CUD
CUD
EPF
CUD
IFN
CUD
CUD
Awaji Island, Japan
Oudekraal, South Africa
Oudekraal, South Africa
Shark Bay, Australia
Scotland
Shark Point, Australia
Baltic & North Sea, Germany
Sydney, Australia
Bare Island, Australia
Bare Island, Australia
Shark Point, Australia
Awaji Island, Japan
Auckland, New Zealand
Anjuna & Baga, India
San Sebastian, Spain
Morib Beach, Malaysia
Israel
Anjuna & Baga, India
Tuandao Bay, China
Sea of Japan, Russia
Philippines & Japan
Awaji Island, Japan
Auckland, New Zealand
Tolo, Hong Kong
Vellar Estuary, India
CUD
EPF
INF
IFN
CUD, SEM
CUD
CUD, SEM
SEM
CUD
CUD
CUD
DGGE
CUD
CUD
CUD
SEM
IFN
CUD
CUD
CUD, SEM
CUD
CUD
CFISH
CUD, SEM
CUD
CUD, DGGE
CUD
CUD
STE
SEM, CUD
Anjuna & Baga, India
Philippines & Japan
Philippines
Auckland, New Zealand
Bicheno, Tasmania
Awaji Island, Japan
Bicheno, Tasmania
South Africa
Awaji Island, Japan
Scotland
Pleubian, France
Baltic & North Sea, Germany
Awaji Island, Japan
Skagerrak, Sweden
Tolo, Hong Kong
Camp Varnum, RI, USA
Baltic Sea, Germany
Tuandao Bay, China
San Jorge Gulf, Argentina
Jiaozhou, China
Oono-Chyo, Japan
Japan
Shark Point, Australia
Jiaozhou, China
Awaji Island, Japan
China
Skagerrak, Sweden
Awaji Island, Japan
Oudekraal, South Africa
Oudekraal, South Africa
Kanagasabhapathy et al. (2008)
Johnson et al. (1971)
Johnson et al. (1991)
Huggett et al. (2006)
Boyd et al. (1999a,b)
Tujula et al. (2006)
Lachnit et al. (2009)
Burke et al. (2009), Delbridge et al. (2004)
Longford et al. (2007)
Penesyan et al. (2009)
Tujula et al. (2006)
Kanagasabhapathy et al. (2008)
Booth & Hoppe (1985)
Ramaiah & Chandramohan (1992)
Genilloud et al. (1994)
Musa & Wei (2008)
Weinberger et al. (1997)
Ramaiah & Chandramohan (1992)
Wang et al. (2009)
Beleneva & Zhukova (2006)
Largo et al. (1997)
Kanagasabhapathy et al. (2008)
Booth & Hoppe (1985)
Kong & Chan (1979)
Lakshmanaperumalsamy &
Purushothaman (1982)
Ramaiah & Chandramohan (1992)
Largo et al. (1997)
Largo et al. (1998)
Booth & Hoppe (1985)
Lewis et al. (1985)
Kanagasabhapathy et al. (2008)
Lewis et al. (1985)
Barreto & Meyer (2006)
Kanagasabhapathy et al. (2008)
Boyd et al. (1999a,b)
Liot et al. (1993)
Lachnit et al. (2009)
Kanagasabhapathy et al. (2008)
Nylund et al. (2008)
Kong & Chan (1979)
Sieburth & Tootle (1981)
Booth & Hoppe (1985)
Wang et al. (2009)
Estevao Belchior et al. (2003)
Duan et al. (1995)
Tsukidate (1971)
Shiba & Taga (1980)
Tujula et al. (2006)
Duan et al. (1995)
Kanagasabhapathy et al. (2008)
Yang et al. (2008)
Nylund et al. (2008)
Kanagasabhapathy et al. (2008)
Johnson et al. (1971)
Johnson et al. (1991)
Coralline algae
Corallina officinalis
Delesseria sanguinea
Delisea pulchra
Gelidium amansii
Gelidium caulacantheum
Gelidium pusillum
Gelidium sp.
Gracilaria changii
Gracilaria conferta
Gracilaria corticata
Gracilaria textorii
Gracilaria verrucosa
Gracilaria spp.
Grateloupia filicina
Hormosira banksii
Hypnea charoides
Hypnea sp.
Hypnea valentiae
Kappaphycus alvarezii
Laurencia distichophylla
Lithophyllum sp.
Lomentaria catenata
Mesophyllum sp.
Osmundaria serrata
Pachymeniopsis lauceolata
Palmaria palmata
Phycodrys rubens
Plocamium telfairiae
Polysiphonia fucoides
Polysiphonia lanosa
Polysiphonia nigrescens
Polysiphonia urceolata
Porphyra columbina
Porphyra haitanensis
Porphyra leucosticta
Porphyra sp.
Porphyra yezoensis
Rhodomela confervoides
Schizymenia dubyi
Sporolithon sp.
Editorial responsibility: Pei-Yuan Qian,
Kowloon, Hong Kong SAR
Submitted: June 10, 2009; Accepted: March 31, 2010
Proofs received from author(s): June 7, 2010