Skip to main content

Advertisement

Log in

Spatio-temporal, environmental factors, and host identity shape culturable-epibiotic fungi of seaweeds in the Red Sea, Egypt

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The study of fungal species diversity from marine algae is in its infancy; as now no studies have been carried out on the distribution and diversity of fungi on the surfaces of marine macroalgae where all fungal–algal interactions tend to begin. The aim of this study was to isolate and describe the culturable part of mycobiota associated with the surface of benthic marine macroalgae (epiphytic or epibiotic fungi). This is an important step in understanding their abundance, diversity and factors influencing their variability and composition. The fungal community was dominated by Ascomycetes (89%) with Eurotiales as the most abundant fungal order followed by Capnodiales, Pleosporales, and Hypocreales, while Zygomycetes was less frequent. The nature of occurrence of fungal genera on different macroalgal hosts suggests that a mix of generalists’ framework applies to fungal epiphytes of seaweeds, but the abundance of fungal taxa varied among ecological functional groups of algae, as well as macroalgal taxonomic groups, which imply host filtering. The fungal assemblages were also characterized by temporal variation with variation in temperature, pH, and salinity as the most important abiotic factors. The structure of fungal assemblages showed high beta diversity and low similarity between hosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anderson, M., R. Gorley & K. Clarke, 2008. Guide to Software and Statistical Methods. PERMANOVA+ for PRIMER University of Auckland and PRIMER-E, Plymouth.

    Google Scholar 

  • Bell, W. & R. Mitchell, 1972. Chemotactic and growth responses of marine bacteria to algal extracellular products. Biological Bulletin 143: 265–277.

    Article  Google Scholar 

  • Bensch, K., U. Braun, J. Z. Groenewald & P. W. Crous, 2012. The genus Cladosporium. Studies in Mycology 72: 1–401.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Booth, C., 1971. The Genus Fusarium. Commonwealth Mycological Institute, Kew, Surrey.

    Google Scholar 

  • Bugni, T. S. & C. M. Ireland, 2004. Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Natural Product Reports 21: 143–163.

    Article  PubMed  CAS  Google Scholar 

  • Damare, S., C. Raghukumar & S. Raghukumar, 2006. Fungi in deep-sea sediments of the Central Indian Basin. Deep Sea Research Part A: Oceanographic Research Papers 53: 14–27.

    Article  Google Scholar 

  • Das, S., P. S. Lyla & S. A. Khan, 2009. Filamentous fungal population and species diversity from the continental slope of Bay of Bengal, India. Acta Oecologica 35: 269–279.

    Article  Google Scholar 

  • Domsch, K., W. Gams & T. Anderson, 1980. Compendium of Soil Fungi, Vol. 1. Academic Press, London.

    Google Scholar 

  • Ellis, M. B., 1971. Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Surrey, Kew.

    Google Scholar 

  • Ellis, M. B., 1976. More Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey.

    Google Scholar 

  • Flewelling, A. J., J. A. Johnson & C. A. Gray, 2013. Isolation and bioassay screening of fungal endophytes from North Atlantic marine macroalgae. Botanica Marina 56: 287–297.

    Article  Google Scholar 

  • Furbino, L. E., V. M. Godinho, I. F. Santiago, F. M. Pellizari, T. M. Alves, C. L. Zani, P. A. Junior, A. J. Romanha, A. G. Carvalho & L. H. Gil, 2014. Diversity patterns, ecology and biological activities of fungal communities associated with the endemic macroalgae across the Antarctic Peninsula. Microbial Ecology 67: 775–787.

    Article  PubMed  Google Scholar 

  • Gunde-Cimerman, N., J. Ramos & A. Plemenitaš, 2009. Halotolerant and halophilic fungi. Mycological Research 113: 1231–1241.

    Article  PubMed  CAS  Google Scholar 

  • Godinho, V. M., L. E. Furbino, I. F. Santiago, F. M. Pellizzari, N. S. Yokoya, D. Pupo, T. M. Alves, P. A. Junior, A. J. Romanha & C. L. Zani, 2013. Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. The ISME Journal 7: 1434–1451.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Harder, T., 2008. Marine epibiosis: concepts, ecological consequences and host defence. In Flemming, H.-C., R. Venkatesan, S. P. Murthy & K. Cooksey (eds), Marine and Industrial Biofouling. Springer, Heidelberg: 219–232.

    Google Scholar 

  • Hasegawa, Y., J. L. Martin, M. W. Giewat & J. N. Rooney-Varga, 2007. Microbial community diversity in the phycosphere of natural populations of the toxic alga, Alexandrium fundyense. Environmental Microbiology 9: 3108–3121.

    Article  PubMed  CAS  Google Scholar 

  • Hellio, C., J.-P. Marechal, B. Veron, G. Bremer, A. S. Clare & Y. Le Gal, 2004. Seasonal variation of antifouling activities of marine algae from the Brittany coast (France). Marine Biotechnology 6: 67–82.

    Article  PubMed  CAS  Google Scholar 

  • Hengst, M. B., S. Andrade, B. González & J. A. Correa, 2010. Changes in epiphytic bacterial communities of intertidal seaweeds modulated by host, temporality, and copper enrichment. Microbial Ecology 60: 282–290.

    Article  PubMed  Google Scholar 

  • Höller, U., G. M. König & A. D. Wright, 1999. Three new metabolites from marine-derived fungi of the genera Coniothyrium and Microsphaeropsis. Journal of Natural Products 62: 114–118.

    Article  PubMed  Google Scholar 

  • Hyde, K. D. & K. Soytong, 2007. Understanding microfungal diversity – a critique. Cryptogamie Mycologie 28: 281–289.

    Google Scholar 

  • Issa, A. A., A. F. Hifney, K. M. Abdel-Gawad & M. Gomaa, 2014. Spatio temporal and environmental factors influencing macroalgal β diversity in the Red Sea, Egypt. Botanica Marina 57: 99–110.

    Article  Google Scholar 

  • Jones, E. B. G., 2000. Marine fungi: some factors influencing biodiversity. Fungal Diversity 4: 53–73.

    Google Scholar 

  • Kohlmeyer, J. & E. Kohlmeyer, 1979. Marine Mycology. The Higher Fungi. Academic Press, New York.

    Google Scholar 

  • Kohlmeyer, J. & B. Volkmann-Kohlmeyer, 2003. Marine ascomycetes from algae and animal hosts. Botanica Marina 46: 285–306.

    Article  Google Scholar 

  • Krause, E., A. Wichels, L. Giménez & G. Gerdts, 2013. Marine fungi may benefit from ocean acidification. Aquatic Microbial Ecology 69: 59–67.

    Article  Google Scholar 

  • Krause, E., A. Wichels, L. Giménez, M. Lunau, M. B. Schilhabel & G. Gerdts, 2012. Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PloS One 7: e47035.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lachnit, T., D. Meske, M. Wahl, T. Harder & R. Schmitz, 2011. Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environmental Microbiology 13: 655–665.

    Article  PubMed  Google Scholar 

  • Legendre, P. & M. J. Anderson, 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs 69: 1–24.

    Article  Google Scholar 

  • Liu, J., M. G. Weinbauer, C. Maier, M. Dai & J.-P. Gattuso, 2010. Effect of ocean acidification on microbial diversity and on microbe-driven biogeochemistry and ecosystem functioning. Aquatic Microbial Ecology 61: 291–305.

    Article  Google Scholar 

  • Loque, C. P., A. O. Medeiros, F. M. Pellizzari, E. C. Oliveira, C. A. Rosa & L. H. Rosa, 2010. Fungal community associated with marine macroalgae from Antarctica. Polar Biology 33: 641–648.

    Article  Google Scholar 

  • Matallah-Boutiba, A., N. Ruiz, C. Sallenave-Namont, O. Grovel, J.-C. Amiard, Y. F. Pouchus & Z. Boutiba, 2012. Screening for toxigenic marine-derived fungi in Algerian mussels and their immediate environment. Aquaculture 342: 75–79.

    Article  Google Scholar 

  • Mueller, G. M., G. F. Bills & M. S. Foster, 2004. Biodiversity of Fungi: Inventory and Monitoring Methods. Academic Press, Amsterdam.

    Google Scholar 

  • Nelson, C. E., S. J. Goldberg, L. W. Kelly, A. F. Haas, J. E. Smith, F. Rohwer & C. A. Carlson, 2013. Coral and macroalgal exudates vary in neutral sugar composition and differentially enrich reef bacterioplankton lineages. The ISME Journal 7: 962–979.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nylund, G. M., F. Persson, M. Lindegarth, G. Cervin, M. Hermansson & H. Pavia, 2010. The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defense. FEMS Microbiology Ecology 71: 84–93.

    Article  PubMed  CAS  Google Scholar 

  • Orij, R., S. Brul & G. J. Smits, 2011. Intracellular pH is a tightly controlled signal in yeast. Biochimica et Biophysica Acta (BBA) – General Subjects 1810: 933–944.

    Article  CAS  Google Scholar 

  • Pitt, J. I., 1979. The Genus Penicillium and Its Teleomorphic States Eupenicillium and Talaromyces. Academic press, London.

    Google Scholar 

  • Pitt, J. I. & A. D. Hocking, 2009. Fungi and Food Spoilage. Springer, New York: 53–295.

    Book  Google Scholar 

  • Podani, J., C. Ricotta & D. Schmera, 2013. A general framework for analyzing beta diversity, nestedness and related community-level phenomena based on abundance data. Ecological Complexity 15: 52–61.

    Article  Google Scholar 

  • Rheinheimer, G., 1992. Aquatic Microbiology. Wiley, New York.

    Google Scholar 

  • Sapp, M., A. S. Schwaderer, K. H. Wiltshire, H.-G. Hoppe, G. Gerdts & A. Wichels, 2007. Species-specific bacterial communities in the phycosphere of microalgae? Microbial Ecology 53: 683–699.

    Article  PubMed  Google Scholar 

  • Schmidt, S., E. Costello, D. Nemergut, C. Cleveland, S. Reed, M. Weintraub, A. Meyer & A. Martin, 2007. Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88: 1379–1385.

    Article  PubMed  CAS  Google Scholar 

  • Suryanarayanan, T., 2012. Fungal endosymbionts of seaweeds biology of marine fungi. In Raghukumar, C. (ed.), Biology of Marine Fungi, Progress in Molecular and Subcellular Biology, Vol. 53. Springer, Berlin: 53–69.

    Google Scholar 

  • Suryanarayanan, T., V. Kumaresan & J. Johnson, 1998. Foliar fungal endophytes from two species of the mangrove Rhizophora. Canadian Journal of Microbiology 44: 1003–1006.

    Article  CAS  Google Scholar 

  • Suryanarayanan, T. S., A. Venkatachalam, N. Thirunavukkarasu, J. P. Ravishankar, M. Doble & V. Geetha, 2010. Internal mycobiota of marine macroalgae from the Tamilnadu coast: distribution, diversity and biotechnological potential. Botanica Marina 53: 457–468.

    Article  Google Scholar 

  • Velez, P., M. C. González, E. Rosique-Gil, J. Cifuentes, M. R. Reyes-Montes, S. Capello-García & R. T. Hanlin, 2013. Community structure and diversity of marine ascomycetes from coastal beaches of the southern Gulf of Mexico. Fungal Ecology 6: 513–521.

    Article  Google Scholar 

  • Wahl, M., 1989. Marine epibiosis. I. Fouling and antifouling: some basic aspects. Marine Ecology Progress Series 58: 175–189.

    Article  Google Scholar 

  • Zuccaro, A. & J. I. Mitchell, 2005. Fungal communities of seaweeds. In Dighton, J., J. F. White & P. Oudeman (eds), The Fungal Community, Its Organization and Role in the Ecosystem, 3rd ed. CRC, Taylor and Francis, New York: 533–579.

    Chapter  Google Scholar 

  • Zuccaro, A., B. Schulz & J. I. Mitchell, 2003. Molecular detection of ascomycetes associated with Fucus serratus. Mycological Research 107: 1451–1466.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohamed Gomaa.

Additional information

Handling editor: Jonne Kotta

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdel-Gawad, K.M., Hifney, A.F., Issa, A.A. et al. Spatio-temporal, environmental factors, and host identity shape culturable-epibiotic fungi of seaweeds in the Red Sea, Egypt. Hydrobiologia 740, 37–49 (2014). https://doi.org/10.1007/s10750-014-1935-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-014-1935-0

Keywords

Navigation