Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter June 11, 2018

Microspongium alariae in Alaria esculenta: a widely-distributed non-parasitic brown algal endophyte that shows cell modifications within its host

  • Pedro Murúa

    Pedro Murúa is a former research associate at the Instituto de Acuicultura of the Universidad Austral de Chile (UACh), where he worked on various aspects of seaweed biology, particularly kelp ecology and mariculture. Pedro got his PhD at the University of Aberdeen in 2018. During his postgraduate studies, Pedro worked on the characterization of new algal pathosystems from cell and molecular biology perspectives. Currently, Pedro is a postdoctoral research assistant in molecular algal pathology, Scottish Association for Marine Science.

    ORCID logo EMAIL logo
    , Frithjof C. Küpper

    Frithjof C. Küpper has held the Chair in Marine Biodiversity at the University of Aberdeen (Oceanlab) since 2011. Over the past 27 years, he has studied the biodiversity and biochemistry of marine plants/algae – especially abiotic and biotic stress. He conducted graduate studies at Roscoff and Konstanz for a joint French-German PhD. His research resulted in the finding of iodide serving as an inorganic antioxidant in kelp, the first described from a living system, impacting atmospheric and marine chemistry. A certified scientific diver, Frithjof has worked extensively in the Eastern Mediterranean, South Atlantic (Ascension and Falkland Islands), but also in the Antarctic Peninsula and the Canadian Arctic for algal diversity-related projects.

    , Liliana A. Muñoz

    Liliana A. Muñoz is a PhD student at the University of Aberdeen (UoA). She got her BSc in 2009 working with the mariculture of the giant kelp (Universidad Austral de Chile), and her MSc in 2016, studying cryptic algal biodiversity from Easter Island (UoA). Presently, Liliana is working on the molecular characterization of parasitic stramenopiles of marine molluscs.

    , Miriam Bernard

    Miriam Bernard is a PhD candidate at Roscoff Marine Station. She obtained her Master’s degree from the University of Bonn and the Alfred Wegener Institute, Bremerhaven working on the impact of global change and interspecific competition on Arctic kelps. Her current research focusses on the interaction of kelps with filamentous algal endophytes.

    and Akira F. Peters

    Akira F. Peters is a gentleman scientist in his enterprise Bezhin Rosko at Santec, Brittany, France. He obtained a PhD from Konstanz University in 1986. He likes macroalgae, with a research focus on brown algae, and has worked as post-doc, assistant and associate university professor in Chile, the Netherlands, Germany and France. He is a member of the Marine Biological Association (MBA) and honorary research fellow at the University of Aberdeen.

From the journal Botanica Marina

Abstract

Alaria esculenta is an important kelp species in northern Europe, Atlantic Canada and USA and the Arctic, with high economic potential. Microspongium alariae, a brown algal endophyte using A. esculenta as host, is reported for the first time from Scotland (Great Britain) and Brittany (France), suggesting a wide distribution in NW Europe. The alga was found growing epi-endophytically in A. esculenta stipes and was occasionally associated with warts. Isolated Microspongium thalli grew in host-free cultures and formed plurilocular sporangia in a broad range of temperature and irradiance conditions. DNA barcoding using the nuclear ribosomal ITS1, the mitochondrial COI and the plastidial rbcL confirmed the identity of the endophyte as M. alariae. Electron microscopy was used to compare the alga when endophytic in Alaria with a host-free culture. As an endophyte, cell diameter, pyrenoid diameter and cell wall thickness were reduced. In contrast, there were more plasmodesma connections between endophyte cells, possibly to enhance nutrient transport along the endophytic thallus. In the light of this evidence, a parasitic life style is considered unlikely for the species and the adaptive value of endophytism in M. alariae remains to be elucidated.

About the authors

Pedro Murúa

Pedro Murúa is a former research associate at the Instituto de Acuicultura of the Universidad Austral de Chile (UACh), where he worked on various aspects of seaweed biology, particularly kelp ecology and mariculture. Pedro got his PhD at the University of Aberdeen in 2018. During his postgraduate studies, Pedro worked on the characterization of new algal pathosystems from cell and molecular biology perspectives. Currently, Pedro is a postdoctoral research assistant in molecular algal pathology, Scottish Association for Marine Science.

Frithjof C. Küpper

Frithjof C. Küpper has held the Chair in Marine Biodiversity at the University of Aberdeen (Oceanlab) since 2011. Over the past 27 years, he has studied the biodiversity and biochemistry of marine plants/algae – especially abiotic and biotic stress. He conducted graduate studies at Roscoff and Konstanz for a joint French-German PhD. His research resulted in the finding of iodide serving as an inorganic antioxidant in kelp, the first described from a living system, impacting atmospheric and marine chemistry. A certified scientific diver, Frithjof has worked extensively in the Eastern Mediterranean, South Atlantic (Ascension and Falkland Islands), but also in the Antarctic Peninsula and the Canadian Arctic for algal diversity-related projects.

Liliana A. Muñoz

Liliana A. Muñoz is a PhD student at the University of Aberdeen (UoA). She got her BSc in 2009 working with the mariculture of the giant kelp (Universidad Austral de Chile), and her MSc in 2016, studying cryptic algal biodiversity from Easter Island (UoA). Presently, Liliana is working on the molecular characterization of parasitic stramenopiles of marine molluscs.

Miriam Bernard

Miriam Bernard is a PhD candidate at Roscoff Marine Station. She obtained her Master’s degree from the University of Bonn and the Alfred Wegener Institute, Bremerhaven working on the impact of global change and interspecific competition on Arctic kelps. Her current research focusses on the interaction of kelps with filamentous algal endophytes.

Akira F. Peters

Akira F. Peters is a gentleman scientist in his enterprise Bezhin Rosko at Santec, Brittany, France. He obtained a PhD from Konstanz University in 1986. He likes macroalgae, with a research focus on brown algae, and has worked as post-doc, assistant and associate university professor in Chile, the Netherlands, Germany and France. He is a member of the Marine Biological Association (MBA) and honorary research fellow at the University of Aberdeen.

Acknowledgements

We greatly appreciated field assistance by Martina Strittmatter (SAMS), Françoise Duchemin and Elodie Gahinet (ALEOR) for sampling at Seil Island and Ile Grande, respectively, technical support during laboratory experiments by Dawn Shewring (Oceanlab) and Debbie Wilkinson (Aberdeen Microscopy Facility), and comments from Aldo Asensi regarding TEM. PM was funded by Conicyt (BecasChile no. 41972130422) for PhD studies at the University of Aberdeen, and by the NERC IOF Pump-priming (GlobalSeaweed, scheme NE/L013223/1) for activities at the Scottish Association for Marine Sciences. Endophyte isolation and identification in Brittany was facilitated by the projects IDEALG (France: ANR-10-BTBR-04) and ALFF, respectively. This project has received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement number 624575. We are also grateful for funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland). MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions.

References

Altschul, S.F., T.L. Madden, A.A. Schäffer, J. Zhang, Z. Zhang, W. Miller and D.J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402.10.1093/nar/25.17.3389Search in Google Scholar PubMed PubMed Central

Apt, K.E. 1988. Galls and tumor-like growths on marine macroalgae. Dis. Aquat. Organ. 4: 211–217.10.3354/dao004211Search in Google Scholar

Araújo, P.G., É.C. Schmidt, M.G. Kreusch, C.H. Kano, S.M.P.B. Guimarães, Z.L. Bouzon, M.T. Fujii and N.S. Yokoya. 2014. Ultrastructural, morphological, and molecular characterization of Colaconema infestans (Colaconematales, Rhodophyta) and its host Kappaphycus alvarezii (Gigartinales, Rhodophyta) cultivated in the Brazilian tropical region. J. Appl. Phycol. 26: 1953–1961.10.1007/s10811-014-0348-9Search in Google Scholar

Barrington, K., T. Chopin and S. Robinson. 2009. Integrated multi-trophic aquaculture (IMTA) in marine temperate waters. FAO Fisheries and Aquaculture Technical Paper. No. 529. In: (D. Soto, ed) Integrated mariculture: a global review. FAO, Rome. pp. 7–46.Search in Google Scholar

Blouin, N.A. and C.E. Lane. 2012. Red algal parasites: models for a life history evolution that leaves photosynthesis behind again and again. BioEssays 34: 226–235.10.1002/bies.201100139Search in Google Scholar PubMed

Burkhardt, E. and A.F. Peters. 1998. Molecular evidence from nrDNA ITS sequences that Laminariocolax (Phaeophyceae, Ectocarpales sensu lato) is a worldwide clade of closely related kelp endophytes. J. Phycol. 34: 682–691.10.1046/j.1529-8817.1998.340682.xSearch in Google Scholar

Chapman, A.S., P. Stévant and W.E. Larssen. 2015. Food or fad? Challenges and opportunities for including seaweeds in a Nordic diet. Bot. Mar. 58: 423–433.10.1515/bot-2015-0044Search in Google Scholar

Correa, J.A. 1994. Infections by pigmented algal endophytes: misuse of concepts and terminology. Rev. Chil. Hist. Nat. 67: 5–8.Search in Google Scholar

Dayton, P.K. 2006. Ecology of Kelp Communities. Annu. Rev. Ecol. Syst. 16: 1–33.10.1146/annurev.es.16.110185.001243Search in Google Scholar

Eggert, A., A.F. Peters and F.C. Küpper. 2010. The potential impact of climate change on endophyte infections in kelp sporophytes. In: (A. Israel, R. Einav and J. Seckbach, eds) Seaweeds and their role in globally changing environments. Springer Netherlands, Amsterdam. pp. 139–154.10.1007/978-90-481-8569-6_9Search in Google Scholar

Gachon, C.M.M., M. Strittmatter, D.G. Müller, J. Kleinteich and F.C Küpper. 2009. Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal. Appl. Environ. Microbiol. 75: 322–328.10.1128/AEM.01885-08Search in Google Scholar PubMed PubMed Central

Gachon, C.M.M., T. Sime-Ngando, M. Strittmatter, A. Chambouvet and G.H. Kim. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15: 633–640.10.1016/j.tplants.2010.08.005Search in Google Scholar PubMed

Goff, L.J. 1979. The Biology of Harveyella mirabilis (Cryptonemiales, Rhodophyceae). Vi. Translocation of Photoassimilated 14C2. J. Phycol. 15: 82–87.10.1111/j.1529-8817.1979.tb02966.xSearch in Google Scholar

Guiry, M.D. and G.M. Guiry. 2017. Alaria esculenta. AlgaeBase. World-wide Electron. Publ. Natl. Univ. Ireland, Galw. Searched on the 29th September 2017.Search in Google Scholar

Hardy, G. and M.D. Guiry. 2003. A check-list and atlas of the seaweeds of Britain and Ireland. British Phycological Society, London. p. 421.Search in Google Scholar

Hauck, F. 1884. Die Meeresalgen Deutschlands und Österreichs. In: (L. Rabenhorst, ed) Kryptogamen-Flora von Deutschland, Österreich und der Schweiz, Zweite Auflage. Eduard Kummer, Leipzig. pp. 321–512.Search in Google Scholar

Heesch, S. 2005. Endophytic Phaeophyceae from New Zealand. PhD Thesis, University of Otago, Dunedin. pp. 365.Search in Google Scholar

Heesch, S. and A.F. Peters. 1999. Scanning electron microscopy observation of host entry by two brown algae endophytic in Laminaria saccharina (Laminariales, Phaeophyceae). Phycol. Res. 47: 1–5.10.1111/j.1440-1835.1999.tb00277.xSearch in Google Scholar

Heesch, S., A.F. Peters, J.E. Broom and C.L. Hurd. 2008. Affiliation of the parasite Herpodiscus durvillaeae (Phaeophyceae) with the Sphacelariales based on DNA sequence comparisons and morphological observations. Eur. J. Phycol. 43: 283–295.10.1080/09670260801911157Search in Google Scholar

Howe, M.A. 1914. The marine algae of Peru. Mem. Torrey Bot. Club 15: 1–185.10.5962/bhl.title.97549Search in Google Scholar

Jaasund, E. 1965. Aspects of the marine algal vegetation of North Norway. Bot. Gothobg. 4: 1–174.Search in Google Scholar

Katoh, K. and D.M. Standley. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772–780.10.1093/molbev/mst010Search in Google Scholar PubMed PubMed Central

Kawai, H., T. Hanyuda, S.G.A. Draisma and D.G. Müller. 2007. Molecular phylogeny of Discosporangium mesarthrocarpum (Phaeophyceae) with a reinstatement of the order Discosporangiales. J. Phycol. 43: 186–194.10.1111/j.1529-8817.2006.00308.xSearch in Google Scholar

Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Meintjes and A. Drummond. 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.10.1093/bioinformatics/bts199Search in Google Scholar PubMed PubMed Central

Koch, R. 1882. Die Aetiologie der Tuberculose (Nach einem in der physiologischen Gesellschaft zu Berlin am 24. März cr. gehaltenen Vortrage). Berl. Klin. Wochenschr. 19: 221.Search in Google Scholar

Kohlmeyer, J. 1968. Revisions and descriptions of algicolous marine fungi. Phytopathol. Zeitschrift 63: 341–363.10.1111/j.1439-0434.1968.tb02399.xSearch in Google Scholar

Kohlmeyer, J. and E. Kohlmeyer. 1979. Marine mycology: the higher fungi. Academic Press, London.Search in Google Scholar

Küpper, F.C., A.F. Peters, D.M. Shewring, M.D.J. Sayer, A. Mystikou, H. Brown, E. Azzopardi, O. Dargent, M. Strittmatter, D. Brennan, A.O. Asensi, P. van West and R.T. Wilce. 2016. Arctic marine phytobenthos of northern Baffin Island. J. Phycol. 52: 532–549.10.1111/jpy.12417Search in Google Scholar PubMed PubMed Central

Lane, C.E., C. Mayes, L.D. Druehl and G.W. Saunders. 2006. A multi-gene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. J. Phycol. 42: 493–512.10.1111/j.1529-8817.2006.00253.xSearch in Google Scholar

Lane, C.E., S.C Lindstrom and G.W. Saunders. 2007. A molecular assessment of northeast Pacific Alaria species (Laminariales, Phaeophyceae) with reference to the utility of DNA barcoding. Mol. Phylogenet. Evol. 44: 634–648.10.1016/j.ympev.2007.03.016Search in Google Scholar

Leonardi, P.I., A.B. Miravalles, S. Faugeron, V. Flores, J. Beltrán and J.A. Correa. 2006. Diversity, phenomenology and epidemiology of epiphytism in farmed Gracilaria chilensis (Rhodophyta) in northern Chile. Eur. J. Phycol. 41: 247–257.10.1080/09670260600645659Search in Google Scholar

López Barreiro, D., M. Beck, U. Hornung, F. Ronsse, A. Kruse and W. Prins. 2015. Suitability of hydrothermal liquefaction as a conversion route to produce biofuels from macroalgae. Algal Res. 11: 234–241.10.1016/j.algal.2015.06.023Search in Google Scholar

Loureiro, R., C.M.M. Gachon and C. Rebours. 2015. Seaweed cultivation: potential and challenges of crop domestication at an unprecedented pace. New Phytol. 206: 489–492.10.1111/nph.13278Search in Google Scholar

Mouritsen, O.G. 2013. Seaweeds: edible, available and sustainable. The University of Chicago Press, Chicago. p. 287.10.7208/chicago/9780226044538.001.0001Search in Google Scholar

Munda, I.M. and K. Lüning. 1977. Growth performance of Alaria esculenta off Helgoland. Helgoländer wiss. Meeresunters 29: 311–314.10.1007/BF01614267Search in Google Scholar

Murúa, P., F. Goecke, R. Westermeier, P. van West, F.C. Küpper and S. Neuhauser. 2017. Maullinia braseltonii sp. nov. (Rhizaria, Phytomyxea, Phagomyxida): a cyst-forming parasite of the bull kelp Durvillaea spp. (Stramenopila, Phaeophyceae, Fucales). Protist 168: 468–480.10.1016/j.protis.2017.07.001Search in Google Scholar

Pedersen, P.M. 1981. The life histories in culture of the brown algae Gononema alariae sp. nov. and G. aecidiodides comb. nov. from Greenland. Nord. J. Bot. 1: 263–270.10.1111/j.1756-1051.1981.tb00695.xSearch in Google Scholar

Peters, A.F. 2003. Molecular identification, distribution and taxonomy of brown algal endophytes, with emphasis on species from Antarctica. Proc. 17th Int. Seaweed Symp. 302: 293–302.Search in Google Scholar

Peters, A.F. and M.E. Ramírez. 2001. Molecular phylogeny of small brown algae, with special reference to the systematic position of Caepidium antarcticum (Adenocystaceae, Ectocarpales). Cryptogam. Algol. 22: 187–200.10.1016/S0181-1568(01)01062-5Search in Google Scholar

Peters, A.F., L. Couceiro, K. Tsiamis, F.C. Küpper and M. Valero. 2015. Barcoding of cryptic stages of marine brown algae isolated from incubated substratum reveals high diversity in Acinetosporaceae (Ectocarpales, Phaeophyceae). Cryptogam. Algol. 36: 3–29.10.7872/crya.v36.iss1.2015.3Search in Google Scholar

Ronquist, F., M. Teslenko, P. Van Der Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard and J.P. Huelsenbeck. 2012. Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.10.1093/sysbio/sys029Search in Google Scholar PubMed PubMed Central

Russell, G. 1964. Laminariocolax tomentosoides on the Isle of Man. J. Mar. Biol. Assoc. United Kingdom 44: 601.10.1017/S0025315400027806Search in Google Scholar

Salomaki, E.D. and C.E. Lane. 2014. Are all red algal parasites cut from the same cloth? Acta Soc. Bot. Pol. 83: 369–375.10.5586/asbp.2014.047Search in Google Scholar

Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D.J. White, V. Hartenstein, K. Eliceiri, P. Tomancak and A. Cardona. 2012. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9: 676–682.10.1038/nmeth.2019Search in Google Scholar PubMed PubMed Central

Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.10.1093/bioinformatics/btu033Search in Google Scholar PubMed PubMed Central

Starr, R.C. and J.A. Zeikus. 1993. UTEX-the culture collection of algae at the University of Texas at Austin 1993. List of cultures. J. Phycol. 29: 1–106.10.1111/j.0022-3646.1993.00001.xSearch in Google Scholar

Tai, V., S.C. Lindstrom and G.W. Saunders. 2001. Phylogeny of the Dumontiaceae (Gigartinales, Rhodophyta) and associated families based on SSU rDNA and internal transcribed spacer sequence data. J. Phycol. 37: 184–196.10.1046/j.1529-8817.2001.037001184.xSearch in Google Scholar

Villalard-Bohnsack, M. 1995. Illustrated key to the seaweeds of New England. The Rhode Island Natural History Survey, Kingston. p. 144.Search in Google Scholar

Westermeier, R., D.J. Patiño, P. Murúa and D.G. Müller. 2011. Macrocystis mariculture in Chile: growth performance of heterosis genotype constructs under field conditions. J. Appl. Phycol. 23: 819–825.10.1007/s10811-010-9581-zSearch in Google Scholar

Wickham, H. 2009. ggplot2. Springer-Verlag New York, New York.10.1007/978-0-387-98141-3Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2017-0095).


Received: 2017-11-06
Accepted: 2018-05-17
Published Online: 2018-06-11
Published in Print: 2018-07-26

©2018 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 3.5.2024 from https://www.degruyter.com/document/doi/10.1515/bot-2017-0095/pdf
Scroll to top button