Microbial Bioactives

Microbial Bioactives | Online ISSN 2209-2161
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Life at the Edge: Marine Fungi and Microbial Resilience in Deep-Sea Hypersaline Anoxic Basins

Abstract 1. Introduction 2. Materials and Methods 3. Results 4. Discussion 5. Limitations 6. Conclusion Author Contributions References

Armania Nurdin 1*

+ Author Affiliations

Microbial Bioactives 6 (1) 1-17 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) remain among the most physically and chemically extreme habitats known in the marine environment, yet growing evidence suggests that these ecosystems are far more biologically dynamic than previously assumed. This review synthesizes current knowledge regarding fungal diversity, ecological functioning, and adaptive survival strategies within DHAB systems, with particular emphasis on the Mediterranean and Red Sea basins. Drawing from molecular surveys, cultivation-based investigations, microscopy, and meta-analytical interpretations, the study reveals that fungal communities are not merely transient occupants of these environments but active contributors to deep-sea ecosystem processes. The halocline consistently emerged as a biologically enriched transition zone where fungal abundance and diversity increase alongside organic matter accumulation and steep redox gradients. Fungi appear to persist through a combination of osmoregulatory mechanisms, stress-response pathways, and metabolic flexibility that enable survival under permanent anoxia, extreme salinity, and high hydrostatic pressure. Beyond ecological significance, DHAB-associated fungi also represent a promising yet largely unexplored reservoir of extremozymes and secondary metabolites with potential applications in biotechnology, pharmaceuticals, and industrial bioprocessing. Although methodological heterogeneity and limited geographic coverage still constrain interpretation, the collective evidence increasingly challenges long-standing assumptions that deep hypersaline systems are biologically marginal. Instead, DHABs emerge as critical natural laboratories for understanding microbial resilience, biogeochemical adaptation, and the broader limits of eukaryotic life under extreme environmental stress.

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

Barone, G., Varrella, S., Tangherlini, M., Rastelli, E., Dell’Anno, A., Danovaro, R., & Corinaldesi, C. (2019). Marine fungi: Biotechnological perspectives from deep-hypersaline anoxic basins. Diversity, 11(7), 113. https://doi.org/10.3390/d11070113       

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., & Bernhard, J. M. (2013). Heterotrophic protists in hypersaline microbial mats and deep hypersaline basin water columns. Life, 3(2), 346-362. https://doi.org/10.3390/life3020346              

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

Forster, D., Qu, Z., Pitsch, G., Bruni, E. P., Kammerlander, B., Pröschold, T., Sonntag, B., Posch, T., & Stoeck, T. (2021). Lake ecosystem robustness and resilience inferred from a climate-stressed protistan plankton network. Microorganisms, 9(3), 549. https://doi.org/10.3390/microorganisms9030549          

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

Hoerstmann, C., Wohlrab, S., & John, U. (2022). Concepts towards functional eukaryotic microbial biogeography in the ocean. Journal of Marine Science and Engineering, 10(11), 1730. https://doi.org/10.3390/jmse10111730       

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

Liu, Y., He, H., Fu, L., Liu, Q., Yang, Z., & Zhen, Y. (2019). Environmental DNA sequencing reveals a highly complex eukaryote community in Sansha Yongle Blue Hole, Xisha, South China Sea. Microorganisms, 7(12), 624. https://doi.org/10.3390/microorganisms7120624          

Malygina, A., Balkin, A., Polyakova, E., Stefanov, S., Potekhin, A., & Gogoleva, N. (2023). Taxonomic diversity of the microbial biofilms collected along the thermal streams on Kunashir Island. Ecologies, 4(1), 106-123. https://doi.org/10.3390/ecologies4010009       

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

Mitrovic, M., Cackovic, A., Selak, L., Markovic, T., & Orlic, S. (2025). A preliminary study on the eukaryotic microbial diversity in Croatian geothermal waters. Water, 17(4), 541. https://doi.org/10.3390/w17040541

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

Schoenle, A., Jeuck, A., Nitsche, F., Venter, P., Prausse, D., & Arndt, H. (2016). Methodological studies on estimates of abundance and diversity of heterotrophic flagellates from the deep-sea floor. Journal of Marine Science and Engineering, 4(1), 22. https://doi.org/10.3390/jmse4010022

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

Weisbrod, B., Wood, S. A., Steiner, K., Whyte-Wilding, R., Puddick, J., Laroche, O., & Dietrich, D. R. (2020). Is a central sediment sample sufficient? Exploring spatial and temporal microbial diversity in a small lake. Toxins, 12(9), 580. https://doi.org/10.3390/toxins12090580           

Wu, S., Zhao, W., Liu, M., Gao, F., & Chen, H. (2023). Prokaryotic and eukaryotic communities characteristic in the water column and sediment along the Xiangjiang River, China. Water, 15(12), 2189. https://doi.org/10.3390/w15122189       

Yakimov, M. M., Giuliano, L., Cappello, S., Denaro, R., & Golyshin, P. N. (2007a). 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. (2007b). Primary producing prokaryotic communities of deep anoxic lake L’Atalante. ISME Journal, 1(8), 743–755. https://doi.org/10.1038/ismej.2007.83


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