J Appl Phycol (2009) 21:11–18
DOI 10.1007/s10811-007-9298-9
Epi-endophytic symbiosis between Laminariocolax
aecidioides (Ectocarpales, Phaeophyceae) and Undaria
pinnatifida (Laminariales, Phaeophyceae) growing
on Argentinian coasts
M. Cecilia Gauna & Elisa R. Parodi & Eduardo J. Cáceres
Received: 28 March 2007 / Revised and Accepted: 3 December 2007 / Published online: 22 January 2008
# Springer Science + Business Media B.V. 2007
Abstract The present is the first study on epi-endophytic
algae on thalli of Undaria pinnatifida growing along
Argentinian coasts. The main goal is to describe the nature
and the morphology of this symbiosis. Individuals of
Laminariocolax aecidioides were detected in both June
and December 2004, growing on U. pinnatifida sporophytes. In nature, the epi-endophyte were macroscopically
observed as dark zones that partially covered the hosts’
fronds. L. aecidioides vegetative thalli were irregularly
branched uniseriate filaments. The life cycle is described
from laboratory cultures started from Patagonian populations. Caryology revealed that the sporophytic diploid
phase presented 16 chromosomes whereas the gametophytic haploid phase presented 8 chromosomes. Isolates made
from thalli growing in the interior of infected hosts
developed into filamentous, branched sporophytes that
reproduced by both unispores and plurispores that were
produced in unilocular and plurilocular sporangia, respec-
M. C. Gauna : E. R. Parodi
Laboratorio de Ecología Acuática,
Universidad Nacional del Sur-Instituto
Argentino de Oceanografía (CONICET),
8000 Bahía Blanca, Argentina
E. J. Cáceres
Laboratorio de Ficología y Micología,
Universidad Nacional del Sur,
CIC. 8000 Bahía Blanca, Argentina
M. C. Gauna (*)
Laboratorio de Ficología,
Instituto de Argentino de Oceanografía (I.A.D.O.),
Camino Carrindanga Km 7,5,
8000 Bahía Blanca, Argentina
e-mail: cgauna@criba.edu.ar
tively. The results of this paper also allowed us to conclude
that L. aecidioides uses the thalli of U. pinnatifida as a
proper substrate. The penetration of endophitic filaments
among the host´s cortical cells produced a lateral compression and, finally, their thalli development generated
perforations in the host tissues. The effects of the epiendophytic infection of L. aecidioides on U. pinnatifida are
neither severe nor deleterious.
Keywords Argentina . Epi-endophyte algae .
Laminariocolax aecidioides . Phaeophyceae .
Undaria pinnatifida
Introduction
Undaria pinnatifida (Harvey) Suringar 1873 (Laminariales,
Phaeophyceae) is a kelp that show large (ca. 0.5–3.0 m),
annual sporophytes with a lobed lamina with evident
midrib, attached by root-like haptera to rock, stone, wood,
shells, tunicates or sometimes plants and also to most
artificial substrates. U. pinnatifida is widely distributed in
Europe (Floc’h et al. 1991; Fletcher and Manfredi 1995;
Hardy and Guiry 2003); Asia (Tseng 1984; Yoshida et al.
1990; Lee and Yoon 1998); North America (Aguilar-Rosas
et al. 2004); Australia and New Zealand (Hay and Luckens
1987; Adams 1994; Nelson 1999; Womersley 2003).
In December 1992, U. pinnatifida was detected for the
first time in Argentina close to the international harbor of
Puerto Madryn (Piriz and Casas 1994). Thalli were normally
colonized by the microscopic brown epi-endophyte
Laminariocolax aecidioides (Streblonema aecidioides sensu
Yoshida and Akiyama (1979) Ectocarpales, Phaeophyceae),
whose individuals formed a hairy cover on the host surface.
12
The main goals of the present study are: (1) to describe
the bona fide nature and the morphology of the symbiosis
between L. aecidioides and U. pinnatifida in Argentinian
populations; (2) to describe for the first time the morphology
of L. aecidioides under culture conditions; and (3) to find
clues to determine the state of health of the Argentinian U.
pinnatifida community.
In general, most of the morphological studies on
epiphytism refer to infections on red algal hosts of
commercial interest, mainly by green epiphytes (Correa
and McLachlan 1991, 1992, 1994; Correa et al. 1988,
1993, 1994). Comprehensive morphological studies on epiendophytes on brown seaweeds are very scarce.
Thalli of another species of Undaria have been observed
in Europe infected with filaments of L. aecidioides by
Veiga et al. (1997) and the relationship between Undaria
sp. and Streblonema aecidioides (=L. aecidioides) populations has been described on Japanese coasts in the northwest Pacific by Yoshida and Akiyama (1979).
Reports indicate that L. aecidioides filaments also infect
blades of Laminaria saccharina from Greenland (Pedersen
1981), the western Baltic (Burkhardt and Peters 1998) and
the north coast of Spain (South and Tittley 1986; Veiga et
al. 1997), and also blades of Laminaria hyperborea from
the coasts of Helgoland (Lein et al. 1991). Some populations of L. aecidioides found on Hedophyllum sessile have
been mentioned as S. aecidioides by Abbott and Hollenberg
(1976).
Materials and methods
Fronds of Undaria pinnatifida were obtained from intertidal and subtidal populations along the coast of Puerto
Madryn, in the province of Chubut, Argentina (42°47′S,
65°02′W) during December 2004.
After being collected, fronds of U. pinnatifida were kept
on ice and retained in labelled plastic bags until they were
examined in the laboratory, usually within 5 h after
collection. Fronds were then brushed and rinsed under
running tap water. Small portions of infected fronds were
sectioned, then immersed in fresh 0.5% solution of sodium
hypochlorite for 30 s, and finally rinsed three times, 5 min
each, in sterile seawater. A 2-min sonication was subsequently applied to 5 × 5 mm portions in sterile seawater,
renewing the seawater after each burst. This cleaning
procedure was followed in order to remove diatoms as
well as other epiphytes.
Crude cultures of L. aecidioides were initiated by
inoculating portions of cleaned fronds U. pinnatifida in
plastic Petri dishes containing PES medium (Provasoli
1968). Cultures were maintained at 21±1° C with an
J Appl Phycol (2009) 21:11–18
illumination regime of 12:12 h LD, with a photon flux
density of 15 μmol photons m−2 s−1. Vegetative endophytic
filaments, and also spores from both plurilocular and
unilocular sporangia, were isolated using the hanging-drop
technique. To avoid further diatoms contamination, a 2.5%
germanium dioxide solution was added to the culture
during the first week (Lewin 1966; Christensen 1982).
Clonal cultures were established by pipetting single
germlings or thallus fragments in advance of first signs of
maturity in the cultures. Strains were maintained for
4 weeks. L. aecidioides filaments formed small 0.1-mm
spherical masses inside excised host tissue after 4 weeks in
culture. No other algae or microorganisms were present.
The filaments were removed and cultured separately for
study.
Cytomorphometry was carried out using a stereoscopic
microscope Wild-Herbrugg and an inverted microscope
Nikon Eclipse TE 300, with anoptral phase contrast and
differential interference contrast (DIC) and with an incorporated camera Nikon FDX 35. The presence or absence of
epi-endophyte filaments was determined under light microscope in semi-thin sections of thalli of U. pinnatifida
obtained with glass knives on a Reicher Ultracut OM U2
ultramicrotome. In order to obtain semi-thin sections, thalli
were fixed in 2.5% glutaraldehyde in seawater for 2 h at
4°C, and postfixed in 1% OsO4 in sea water for 2 h at 4°C.
The material was dehydrated in a graded acetone series and
embedded in Spurr´s low viscosity resin. The resin was
removed using a metallic sodium, benzene and methylic
alcohol solution (Hayat 1986). Sections were stained with a
combination of colorants, namely haematoxiline-malachite
green-basic fucsine (1:1:1) (Berkowitz et al. 1968).
Chromosome counts were carried out using unialgal
cultures of L. aecidioides, derived from biflagellate zoospores. Thalli were fixed either in 1:3 mixture glacial acetic
acid/absolute ethanol or in 6:3:1 mixture formaldehydeabsolute ethanol-glacial acetic acid at 5°C during a period
of 2–24 h. Postfixation was carried out with 70% ethyl
alcohol. The material was subsequently hydrolyzed for
30 min in 1 N HCL at room temperature and stained with
Schiff stain in darkness for 2 h (Johansen 1940). It was
bleached during 20 min in a 1:3:3 mixture of sodium
metasulphite: 1 N HCL: distilled water, washed with
distilled water for 30 min, and finally mounted in a drop
of 2% acetic acid solution of ferric haematoxylin with
added iron acetate (Núñez 1968).
Scanning electron microscopy
Filaments of L. aecidiodes and thallus of U. pinnatifida
were fixed in 2.5% glutaraldehide-seawater at 5°C in
cacodilate buffer for 2 h. They were then mounted on
slides covered with 0.5% poly-D-lysine and dehydrated in a
J Appl Phycol (2009) 21:11–18
graded acetone series. Samples were finally critical point
dried during 1 h, coated with gold, and observed with a Jeol
35 CF scanning electron microscope (SEM).
Results
13
natural conditions. Cells were 25.56 μm (11–55 μm; SD: 5;
n=32) in length and 14.8 μm (10–19 μm; SD: 2.44; n=32)
in diameter (Fig. 2a). Short, erect filaments formed by cells
of smaller dimensions were also observed; their cells
reached 6.28 μm (3.36–11.2 μm; SD: 2.42; n=30) in
diameter and 9.70 μm (4.5–15.7 μm; SD: 3.92; n=30) in
length (Fig. 2b). All cells normally contained 2 discoid
plastids (Fig. 2b).
Morphology of thalli Laminariocolax aecidioides in nature
Reproduction
Infected fronds of Undaria pinnatifida exhibited brown
spots near the mucilage ducts (Fig. 1a). SEM images
revealed the spots were formed by thalli of L. aecidioides
partially covering the surface of the fronds (Fig. 1b,
arrows). Cross-sections of infected U. pinnatifida tallus
showed that thalli L. aecidioides were localized principally
on the cortical zone of the hosts. Thalli of L. aecidioides
were filamentous, uniseriate and branched (Figs. 1c and
1d). They formed a postrate system that reached the medulla
of the host but did not penetrate host cells, thus no necrotic
tissues were present in their vicinity. Filaments exhibited
cells 5–15 μm in diameter and 10–40 μm in length, with one
to several chloroplasts, discoid or band-shaped.
Plurilocular sporangia were solitary, ovoid and uniseriate,
15–20 μm diameter (Fig. 1c, arrows). Unilocular sporangia
were also solitary, ovoid, 7–12 μm in diameter, 20–40 μm
in length (Figs. 1e–1h and 1i); they showed either basal or
apical dehiscence.
Infection
Infected sporophytes did not present their characteristic
healthy brown colour, being smooth and flexible, in
contrast to the non-infected ones, which were darker,
rough, less flexible and curved. The presence of L.
aecidioides also produced perforations in the tissues that
were eventually occupied by vegetative and reproductive
structures of the endophyte (Fig. 1j).
Semi-thin sections of infected thalli showed that U.
pinnatifida cortical cells did not exhibit vertical compression but rather a lateral compression owing to the presence
of L. aecidioides filaments among them.
Also, unidentified epiphytic bacteria distributed throughout all the surface of hosts were normally present in
infected thalli (Fig. 1k).
Characteristics of Laminariocolax aecidioides developing
in culture
Vegetative morphology
Thalli consisted on branched filaments with diffuse growth.
They did not develop hyaline hairs, like those observed in
After a week under culture conditions, filaments developed
terminal and intercalar, cylindrical, unilocular sporangia
(Figs. 2c and 2d). Each unilocular sporangium was 30 μm
(12–42 μm; SD: 8.5; n=15) in length and 14.3 μm (11–
18 μm; SD: 2.45; n=15) in diameter. Unilocular sporangia
formed spherical, biflagellate zoospores, 5-6 μm in diameter, with a lateral chloroplast with an eyespot (Figs. 2e and
2f). Filaments also formed cylindrical, plurilocular sporangia, 49 μm (30–81 μm; SD: 12. 3; n=13) in length and
14.4 μm (7–20; SD: 3.66; n=13) in diameter. Plurilocular
sporangia produced biflagellate zoospores, which were
liberated through an apical porus at maturity (Fig. 2g).
Zoospores, which were negatively phototactic, were pearshaped to ovoid, 5–7 μm×6-5 μm , and possessed one or
two chloroplasts and a single red eyespot.
Thalli bearing both unilocular and plurilocular zoosporangia were placed in hanging-drop cultures. After 2 weeks of
cultivation, new plurilocular sporangia of the same type as
those on the parent thallus were formed. The zoids released
were identical to those described above. Settlement and
germination of zoospores was observed. They developed
into thalli with both unilocular and plurilocular sporangia.
The settlement and early germination of unispores was
not observed. They eventually developed into gametophytes that were morphologically different from the
sporophytes. Adult gametophytes were branched filaments
with diffuse growth that did not develop hyaline hairs.
Filaments exhibited cells 14 μm (5–31 μm; SD: 5.6; n=32)
in length and 8 μm (5–16; SD: 2.62; n=32) in diameter
(Fig. 2h). Cells contained 2–4 discoid chloroplasts, each
one with a conspicuous pyrenoid (Fig. 2h). Gametophytes
also developed branched prostrate filaments constituted by
doliiform cells, 5.26 μm (4–8 μm; SD: 1.16; n=15) in
length and 4.7 μm (4–7 μm; SD: 0.85; n=15) in diameter.
These cells generally contained 2 discoid plastids with only
one pyrenoid (Fig. 2h) At maturity, many of the cells of the
erect filaments were transformed into cylindrical (and both
terminal and intercalar plurilocular) gametangia, 21.9 μm
(5–50 μm; SD: 18.5; n=10) in length and 8.9 μm (5–
13 μm; DS: 2.23; n=10) in diameter (Fig. 2i). Eventually,
4–6 μm× 3–4 μm negatively phototactic isogametes were
released by an apical opening (Fig. 2j).
14
Caryology
Chromosome counts were made in both sporophytic and
gametophytic thalli. Small, cane-shaped chromosomes were
observed placed in very tight prometaphase plates. In the
sporophytes, diploid assemblages of 16 chromosomes were
counted whereas in haploid gametophytes plates of 8 chromosomes were found (Figs. 2k and 2l).
Discussion
Infections by microscopic endophytic brown algae are
common diseases of kelp species. They are known from
various host species in different parts of the world, such as
Japan (Yoshida and Akiyama 1979; Kawai and Tokuyama
1995), Pacific North America (Andrews 1977; Apt 1988),
Europe (Dangeard 1931; Russell 1983a, b; Lein et al. 1991;
Peters and Ellertsdóttir 1996; Peters and Schaffelke 1996;
Heesch and Peters 1999), and Pacific South America
(Peters 1991).
In this study, the only endophyte identified was L.
aecidioides. Except for the strictly parasitic Herpodiscus
durvillaeae (Lindauer) South (South 1974; Peters 1990) on
Durvillea antartica, all brown endophytes so far described
are pigmented (Burkhardt and Peters 1998). In general, and
as in the present case, the epi-endophytes are included in
the “simple brown algae” that is, the “Ectocarpales sensu
lato” (Fritsch 1945; Burkhardt and Peters 1998). Many
were originally identified as Ectocarpus Lyngbye and are
now commonly included in Streblonema (Derbès et Solier
in Castagne (Derbès and Solier 1851). Several other genera,
however, have also been proposed as the identity of these
organisms. These are Entonema Reinsch (1875), Phycocelis
Stroemfelf (Kuckuck 1894), Myrionema Greville
(Sauvageau 1898), Pilocladus Kuckuck (1854), Gononema
Kuckuck et Skottsberg in Skottsberg (Pedersen 1981),
Microspongium Reinke (Pedersen 1984), Laminarionema
Kawai et Tokuyama (Kawai and Tokuyama 1995) and
Laminariocolax Kylin (Kylin 1947). Regarding the Argentinian coasts, the present study is the first made on an epiendophyte of a brown algal host; thus, we are not able to
made comparations with the relationships of L. aecidioides
with thalli of some other kelp species different from U.
pinnatifida. Moreover, in studies on red algae hosts from
Argentina, such as Rhodymenia sp., Hymenena falklandica
(Gauna 2005), and Gracilaria gracilis (Martin et al. 2007),
L. aecidioides has not been mentioned.
Although dramatic morphological effects were observed
in infected hosts of U. pinnatifida, like galls or necrotic
tissues, as a result of the infection, the presence of L.
J Appl Phycol (2009) 21:11–18
Fig. 1 Undaria pinnatifida infected by Laminariocolax aecidioides. b
(a) Dark spots observed on the surface of a blade of U. pinnatifida
(white arrows), symptom of the infection of L. aecidioides. (b) SEM
image showing several thalli of L. aecidioides (arrows) covering
partially the surface of a sporophyte of frond of U. pinnatifida.
(c) Semi-thin transverse sections through an infected frond of U.
pinnatifida to see the location of the L. aecidioides filaments; prostrate
filament of L. aecidioides on the surface of hosts. A plurilocular
sporangium is observed (arrow). (d) Semi-thin transverse sections
through an infected frond of U. pinnatifida to see the location of the L.
aecidioides filaments. A filament of L. aecidioides is observed, which
has penetrated into the cortical zone through intercellular spaces
(arrow). (e) SEM showing a thallus of L. aecidioides with
reproductive structures formed in the erect system (arrows).
(f) SEM, detail of the Fig. 1e image, to show vegetative cells and
reproductive structures located in the erect system. (g) SEM detail of
an empty L. aecidioides unilocular sporangium exhibiting basal and
apical dehiscence, respectively. (h) SEM detail of an empty L.
aecidioides unilocular sporangium exhibiting basal and apical dehiscence, respectively. (i) A semi-thin transverse section of a U.
pinnatifida fronds to see a L. aecidioides filaments. Note a unilocular
sporangium in the prostrate system (arrow). (j) Detail of a perforation
of U. pinnatifida frond caused by the presence of the epi-endophyte.
The central part of the perforation is occupied by reproductive
structures of L. aecidioides. (k) SEM detail of the surface of an
infected frond of U. pinnatifida to show numerous epiphytic bacteria
normally present
aecidioides did not prevent the normal maturation of the
sorus, the production of zoospores and thus the reproductive capacity and biomass augment in U. pinnatifida. In
consequence, we can assume that the effects of the epiendophytic infection of L. aecidioides on U. pinnatifida are
neither severe nor deleterious.
The results of this paper also allowed us to suggest that
L. aecidioides uses the thalli of U. pinnatifida as a proper
substrate, since their thalli developed their entire life cycle
on them.
None of the thalli with dark spots or distorted thalli
lacked endophytes, but more than half of the plants that
contained endophytes did not show macroscopically visible
disease symptoms. The mere presence of endophytes in any
part of the host does not seem to be sufficient for disease
symptoms to develop, and both endophyte density and
distribution in the host may be important. A lag phase
between infection and appearance of a pathological disorder
is usual in infectious diseases and has also been reported by
Peters and Schaffelke (1996) for the endophyte Gononema
aecidioides in Laminaria saccharina in the western Baltic.
The young and adult thalli of U. pinnatifida infected by
L. aecidioides in Argentina presented equal sintomatology
as that described by Yoshida and Akiyama (1979) in
Japanese adult populations of the same species. Nevertheless, individuals of the populations of L. aecidioides
deciphered by Yoshida and Akiyama presented minor
cytological vegetative and reproductive dimensions compared with those of the Argentinian populations.
J Appl Phycol (2009) 21:11–18
The information about how endophytes are transmitted
and the way of penetration in the host’s is scarce. Apt
(1988) has suggested that the epiphytic filaments enter the
internal hosts tissues of these organisms through wounds.
Nevertheless, the observations made in this study on U.
pinnatifida, indicate that L. aecidioides do not require a
wound to gain access to internal tissues, as we observed a
prevalence of penetrations in regions near the openings of
mucilage glands. Kylin (1947) for Lamiraiocolax tomentosoides and Peters and Ellertsdóttir (1996) for Laminarionema elsbetiae suggested that spores are specialized
15
infective agents that attach to and penetrate the healthy
host surface, and they also observed that no wounds or
other openings are required for a successful invasion of the
host.
Chromosomes counts in species of the genus Laminariocolax have not been published so far. For Laminariocolax
macrocystis, there is only the mention of chromosomal
complements of n=13-–5. The present cytological studies of
L. aecidioides determined that the registered n=8 is in the
lower rank of the proposed haploid chromosomal number for
the Ectocarpales (8–13), indicated by Lewis (1996).
16
J Appl Phycol (2009) 21:11–18
The results described here on culture material, in
particular the caryological observations, provide good
evidence that L. aecidioides possesses sexuality and two
different alternating generations. Both generations are
microscopic and perhaps live on the same host. The
sporophyte of L. aecidioides may directly replicate itself
by means of plurispores, but can also produce unispores
that develop into gametophytes. The gametophytes may
form identical male and female gametes to give a new
sporophytic generation.
Taxonomical comments
Fig. 2 Laminariocolax aecidioides in culture. (a) A thallus of L.
aecidioides after 4 weeks in culture. (b) Short, erect filaments of L.
aecidioides, exhibiting doliiforms cells. All cells normally contained 2
discoid plastids. (c) A cylindrical, terminal unilocular sporangium
(arrow), formed in an erect filament. (d) A cylindrical, intercalar
unilocular sporangium (arrow), formed in an erect filament. (e) A
zoosporangium with unispores (arrow). (f) Detail of a biflagellate
unispores. Note, it shows a laterally arranged plastid and eyespot. (g)
Plurilocular sporangium with biflagellated pluripores. Note, it is
cylindrical, uniseriate and that it exhibits an apical pore (arrow). (h)
Gametophyte filament whose cells posses 2-4 discoid plastids (white
arrows), and conspicuous pyrenoids (black arrows). (i) Intercalar,
unilocular immature gametangia in a gametophyte filaments. (j)
Release of isogametes through a single apical pore in each
gametangium (arrows). (k) Haploid metaphase plate with 8 chromosomes. (l) Haploid metaphase plate with 8 chromosomes. Graphical
representation of the metaphase plate
Up to now, four species of Laminariocolax have been
described: L. eckloniae A. F. Peters, L. aecidioides, L.
tomentosoides (Fallow) Kylin and L. macrocystis (A. F.
Peters) A. F. Peters (Burkhardt and Peters 1998). All these
species exhibit the same endophytic habit, but morphological differences exist. However, more significant for the
species definition is the dependability of each species to a
specific host species, i.e. L. tomentosoides colonises several
J Appl Phycol (2009) 21:11–18
species of Laminaria digitata, whereas L. macrocystis lives
on sporophylls and cauloid of Macrocystis pyrifera and L.
eckloniae, in turn colonises thalli of Ecklonia maxima
(Osbeck) Papenfuss (Burkhardt and Peters 1998). L.
aecidioides was mentioned under their different synonyms
in several regions. Although the information is not
complete, since references to hosts were generally not
indicated, it is mainly distributed in the Northern hemisphere. In this work, the distribution of the species is
extended to the Southern hemisphere, being also the first
report for the Atlantic Ocean coasts.
With the exception of one report on the occurrence of a
species of Laminariocolax on the red alga Grateloupia
doryphora (Montagne) Howe (Villalard-Bohnsack and
Harlin 2001), members of this genus were mentioned as
mainly growing on seaweeds of the order Laminariales. L.
aecidioides was also isolated from fronds of L. hyperborea
(Gunnerus) Foslie in Britain, Norway (Lein et al. 1991) and
Helgoland (Ellertsdóttir and Peters 1997), also from
Laminaria digitata frond (Hudson) J. V. Lamouroux in
Maine, (Burkhardt and Peters 1998), Undaria sp. (Yoshida
and Akiyama 1979), Heldophyllum sessile (Areschoug)
Setchell and Gardner (1922) (Abbott and Hollenberg 1976)
and recently from Undaria pinnatifida (Gauna 2005).
Acknowledgements M.C.G. has a fellowship of the Consejo
Nacional de Investigaciones Científicas y Técnicas de la República
Argentina (CONICET). E.R.P. is Research Member of the Consejo
Nacional de Investigaciones Científicas y Técnicas de la República
Argentina (CONICET). E.J.C. is Research Member of the Comisión
de Investigaciones Científicas de la Provincia de Buenos Aires,
República Argentina (CIC). The Secretary of Science and Technology
of the Universidad Nacional del Sur provided funds by grant PGI
CSU-24 B/119 to E.R.P.
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