Microbial Bioactives
Life at the Edge: Marine Fungi and Microbial Resilience in Deep-Sea Hypersaline Anoxic Basins
Armania Nurdin 1*
Microbial Bioactives 6 (1) 1-8 https://doi.org/10.25163/microbbioacts.6110671
Submitted: 18 January 2023 Revised: 21 March 2023 Accepted: 28 March 2023 Published: 30 March 2023
Abstract
Deep-sea hypersaline anoxic basins (DHABs) are among the most extreme and least explored ecosystems on Earth, formed through the dissolution of ancient evaporitic deposits and characterized by permanent anoxia, extreme salinity, high hydrostatic pressure, and steep physicochemical gradients. Once considered inhospitable to life, these basins have emerged as natural laboratories for understanding the limits of biological adaptation. Over the past two decades, systematic investigations combining molecular surveys, microscopy, cultivation-based studies, and meta-analytical syntheses have revealed unexpectedly diverse and metabolically active microbial communities thriving at the brine–seawater interface. While prokaryotes initially dominated scientific attention, fungi are now recognized as integral components of DHAB ecosystems. These organisms exhibit remarkable physiological flexibility, enabling them to withstand osmotic stress, chaotropic salts, and limited water activity through specialized metabolic and regulatory mechanisms. Evidence synthesized from multiple DHAB systems, including basins in the Mediterranean and Red Sea, indicates that fungi play essential roles in organic matter degradation, nutrient remineralization, and carbon cycling under extreme conditions. The halocline, acting as a natural trap for sinking organic particles, provides a concentrated energy source that supports fungal growth and promotes interactions with chemoautotrophic prokaryotes. Beyond their ecological relevance, DHAB-associated fungi represent a largely untapped reservoir of novel enzymes and secondary metabolites with promising applications in biotechnology, medicine, and industry. This systematic synthesis highlights the ecological significance, adaptive strategies, and biotechnological potential of fungal communities in DHABs, underscoring their value for advancing our understanding of life at environmental extremes and for guiding future exploration of extreme marine habitats.
Keywords: Deep-sea hypersaline anoxic basins; extreme environments; marine fungi; halocline; polyextremophiles; blue biotechnology
References
Alexander, E., Stock, A., Breiner, H. W., Behnke, A., Bunge, J., Yakimov, M. M., & Stoeck, T. (2009). Microbial eukaryotes in the hypersaline anoxic L’Atalante deep-sea basin. Environmental Microbiology, 11(2), 360–381. https://doi.org/10.1111/j.1462-2920.2008.01777.x
Antunes, A., Ngugi, D. K., & Stingl, U. (2011). Microbiology of the Red Sea (and other) deep-sea anoxic brine lakes. Environmental Microbiology Reports, 3(4), 416–433. https://doi.org/10.1111/j.1758-2229.2011.00264.x
Backer, H., & Schoell, M. (1972). New deeps with brines and metalliferous sediments in the Red Sea. Nature Physical Science, 240, 153–158. https://doi.org/10.1038/physci240153a0
Bernhard, J. M., Kormas, K., Pachiadaki, M. G., Rocke, E., & Edgcomb, V. P. (2014). Benthic protists and fungi of Mediterranean deep hypersaline anoxic basin redoxcline sediments. Frontiers in Microbiology, 5, 1–13. https://doi.org/10.3389/fmicb.2014.00605
Cantrell, S. A., Casillas-Martínez, L., & Molina, M. (2006). Characterization of fungi from hypersaline environments of solar salterns. Mycological Research, 110(8), 962–970. https://doi.org/10.1016/j.mycres.2006.06.005
Charnock, H. (1964). Anomalous bottom water in the Red Sea. Nature, 203, 591. https://doi.org/10.1038/203591a0
Cita, M. B. (2006). Exhumation of Messinian evaporites in the deep sea and creation of deep anoxic brine-filled collapsed basins. Sedimentary Geology, 188–189, 357–378. https://doi.org/10.1016/j.sedgeo.2006.03.013
Corinaldesi, C., Barone, G., Marcellini, F., Dell’Anno, A., & Danovaro, R. (2017). Marine microbial-derived molecules and their potential use. Marine Drugs, 15(4), 118. https://doi.org/10.3390/md15040118
Danovaro, R., Corinaldesi, C., Dell’Anno, A., & Snelgrove, P. V. R. (2017). The deep sea under global change. Current Biology, 27(11), R461–R465. https://doi.org/10.1016/j.cub.2017.02.046
Danovaro, R., Dell’Anno, A., Pusceddu, A., Gambi, C., Heiner, I., & Kristensen, R. M. (2010). The first metazoa living in permanently anoxic conditions. BMC Biology, 8, 30. https://doi.org/10.1186/1741-7007-8-30
Danovaro, R., Snelgrove, P. V. R., & Tyler, P. (2014). Challenging the paradigms of deep-sea ecology. Trends in Ecology & Evolution, 29(8), 465–475. https://doi.org/10.1016/j.tree.2014.06.002
Eder, W., Jahnke, L. L., Schmidt, M., & Huber, R. (2001). Microbial diversity of the brine–seawater interface of the Kebrit Deep, Red Sea. Applied and Environmental Microbiology, 67(7), 3077–3085. https://doi.org/10.1128/AEM.67.7.3077-3085.2001
Eder, W., Ludwig, W., & Huber, R. (1999). Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of Kebrit Deep, Red Sea. Archives of Microbiology, 172(4), 213–218. https://doi.org/10.1007/s002030050762
Edgcomb, V. P., Orsi, W., Breiner, H. W., Stock, A., Filker, S., Yakimov, M. M., & Stoeck, T. (2011). Novel active kinetoplastids associated with hypersaline anoxic basins. Deep Sea Research Part I, 58(10), 1040–1048. https://doi.org/10.1016/j.dsr.2011.07.003
Edgcomb, V. P., Orsi, W., Leslin, C., Epstein, S. S., Bunge, J., & Stoeck, T. (2009). Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins. Extremophiles, 13(1), 151–167. https://doi.org/10.1007/s00792-008-0206-2
Edgcomb, V. P., Pachiadaki, M. G., Mara, P., Kormas, K. A., & Bernhard, J. M. (2016). Gene expression profiling of microbial activities in sediments under haloclines of eastern Mediterranean DHABs. ISME Journal, 10(11), 2643–2657. https://doi.org/10.1038/ismej.2016.58
Gadd, G. M. (Ed.). (2006). Fungi in biogeochemical cycles. Cambridge University Press. https://doi.org/10.1017/CBO9780511550522
Grossart, H. P., Van den Wyngaert, S., Kagami, M., Wurzbacher, C., & Rojas-Jimenez, K. (2019). Fungi in aquatic ecosystems. Nature Reviews Microbiology, 17, 339–354. https://doi.org/10.1038/s41579-019-0175-8
Hallsworth, J. E., Yakimov, M. M., Golyshin, P. N., Gillion, J. L. M., & Timmis, K. N. (2007). Limits of life in MgCl2-containing environments. Environmental Microbiology, 9(3), 801–813. https://doi.org/10.1111/j.1462-2920.2006.01212.x
La Cono, V., Smedile, F., Bortoluzzi, G., Arcadi, E., Maimone, G., Messina, E., & Yakimov, M. M. (2011). Unveiling microbial life in deep-sea hypersaline Lake Thetis. Environmental Microbiology, 13(8), 2250–2268. https://doi.org/10.1111/j.1462-2920.2011.02478.x
Merlino, G., Barozzi, A., Michoud, G., Ngugi, D. K., & Daffonchio, D. (2018). Microbial ecology of deep-sea hypersaline anoxic basins. FEMS Microbiology Ecology, 94(7). https://doi.org/10.1093/femsec/fiy085
Pachiadaki, M. G., Yakimov, M. M., Lacono, V., Leadbetter, E., & Edgcomb, V. (2014). Unveiling microbial activities along the halocline of Thetis. ISME Journal, 8(12), 2478–2489. https://doi.org/10.1038/ismej.2014.100
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., … Moher, D. (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 372, n71. https://doi.org/10.1136/bmj.n71
Sass, A. M., Sass, H., Coolen, M. J. L., Cypionka, H., & Overmann, J. (2001). Microbial communities in the chemocline of a hypersaline deep-sea basin. Applied and Environmental Microbiology, 67(12), 5392–5402. https://doi.org/10.1128/AEM.67.12.5392-5402.2001
Steinle, L., Knittel, K., Felber, N., Casalino, C., de Lange, G., & Lehmann, M. F. (2018). Life on the edge: Active microbial communities in MgCl2-brine basins. ISME Journal, 12(6), 1414–1426. https://doi.org/10.1038/s41396-018-0107-z
Stock, A., Breiner, H. W., Pachiadaki, M., Edgcomb, V., & Stoeck, T. (2012). Microbial eukaryote life in the hypersaline deep-sea basin Thetis. Extremophiles, 16(1), 21–34. https://doi.org/10.1007/s00792-011-0401-4
van der Wielen, P. W. J. J., Bolhuis, H., Borin, S., Daffonchio, D., Corselli, C., Giuliano, L., & Yakimov, M. M. (2005). The enigma of prokaryotic life in deep hypersaline anoxic basins. Science, 307(5706), 121–123. https://doi.org/10.1126/science.1103569
Van Dover, C. L. (2000). The ecology of deep-sea hydrothermal vents. Princeton University Press. https://press.princeton.edu/books/paperback/9780691049298/the-ecology-of-deep-sea-hydrothermal-vents
Wallmann, K., Suess, E., Westbrook, G. H., Winckler, G., & Cita, M. B. (1997). Salty brines on the Mediterranean sea floor. Nature, 387, 31–32. https://doi.org/10.1038/387031a0
Yakimov, M. M., Giuliano, L., Cappello, S., Denaro, R., & Golyshin, P. N. (2007). Microbial community of a hydrothermal mud vent beneath an anoxic brine lake. Origins of Life and Evolution of Biospheres, 37(2), 177–188. https://doi.org/10.1007/s11084-006-9042-4
Yakimov, M. M., La Cono, V., Denaro, R., D’Auria, G., & Giuliano, L. (2007). Primary producing prokaryotic communities of deep anoxic lake L’Atalante. ISME Journal, 1(8), 743–755. https://doi.org/10.1038/ismej.2007.83
Recommended articles
Marine Microbial Metabolites as Bioactive Reservoirs: A Systematic Synthesis of Biosynthetic Diversity and Functional Potential
Risk, Resilience, and Functional Stability of Marine Microzooplankton in a Changing Ocean: Insights from Systematic Review and Meta-Analytical Evidence
Mechanisms of Plant Reproduction: A Comparative Analysis of Sexual and Asexual Methods in Various Plant Species
Save
Citation
View
Share