Abstract

Fungi are phylogenetically and functionally diverse ubiquitous components of almost all ecosystems on Earth, including aquatic environments stretching from high montane lakes down to the deep ocean. Aquatic ecosystems, however, remain frequently overlooked as fungal habitats, although fungi potentially hold important roles for organic matter cycling and food web dynamics. Recent methodological improvements have facilitated a greater appreciation of the importance of fungi in many aquatic systems, yet a conceptual framework is still missing. In this Review, we conceptualize the spatiotemporal dimensions, diversity, functions and organismic interactions of fungi in structuring aquatic food webs. We focus on currently unexplored fungal diversity, highlighting poorly understood ecosystems, including emerging artificial aquatic habitats.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Kagami, M., de Bruin, A., Ibelings, B. W. & Van Donk, E. Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578, 113–129 (2007).

  2. 2.

    Kagami, M., Miki, T. & Takimoto, G. Mycoloop: chytrids in aquatic food webs. Front. Microbiol. 5, 166 (2014).

  3. 3.

    Rasconi, S., Niquil, N. & Sime-Ngando, T. Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic ecosystems. Environ. Microbiol. 14, 2151–2170 (2012).

  4. 4.

    Haraldsson, M. et al. Microbial parasites make cyanobacteria blooms less of a trophic dead end than commonly assumed. ISME J. 12, 1008 (2018).

  5. 5.

    Taylor, D. L. & Sinsabaugh, R. L. in Soil Microbiology, Ecology and Biochemistry (ed. Paul, E. A.) 4th edn 77–109 (Academic Press, 2015).

  6. 6.

    Peay, K. G., Kennedy, P. G. & Talbot, J. M. Dimensions of biodiversity in the Earth mycobiome. Nat. Rev. Microbiol. 14, 434–447 (2016).

  7. 7.

    Shearer, C. A. et al. Fungal biodiversity in aquatic habitats. Biodivers. Conserv. 16, 49–67 (2007).

  8. 8.

    Wurzbacher, C. M., Bärlocher, F. & Grossart, H.-P. Fungi in lake ecosystems. Aquat. Microb. Ecol. 59, 125–149 (2010).

  9. 9.

    Richards, T. A. et al. Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proc. Biol. Sci. 282, 20152243 (2015).

  10. 10.

    Grossart, H.-P. & Rojas-Jimenez, K. Aquatic fungi: targeting the forgotten in microbial ecology. Curr. Opin. Microbiol. 31, 140–145 (2016).

  11. 11.

    Taylor, J. D. & Cunliffe, M. Multi-year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J. 10, 2118–2128 (2016).

  12. 12.

    Park, D. On the ecology of heterotrophic micro-organisms in fresh-water. Mycol. Res. 58, 291–299 (1972).

  13. 13.

    Richards, T. A., Jones, M. D. M., Leonard, G. & Bass, D. Marine fungi: their ecology and molecular diversity. Annu. Rev. Mar. Sci. 4, 495–522 (2012).

  14. 14.

    De Vargas, C. et al. Eukaryotic plankton diversity in the sunlit ocean. Science 348, 1261605 (2015).

  15. 15.

    Debroas, D. et al. Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiol. Ecol. 93, fix023 (2017).

  16. 16.

    Krauss, G.-J. et al. Fungi in freshwaters: ecology, physiology and biochemical potential. FEMS Microbiol. Rev. 35, 620–651 (2011).

  17. 17.

    Fabian, J., Zlatanovic, S., Mutz, M. & Premke, K. Fungal–bacterial dynamics and their contribution to terrigenous carbon turnover in relation to organic matter quality. ISME J. 11, 415–425 (2017).

  18. 18.

    Taube, R., Ganzert, L., Grossart, H.-P., Gleixner, G. & Premke, K. Organic matter quality structures benthic fatty acid patterns and the abundance of fungi and bacteria in temperate lakes. Sci. Total Environ. 610, 469–481 (2018).

  19. 19.

    Nikolcheva, L. G. & Bärlocher, F. Taxon-specific fungal primers reveal unexpectedly high diversity during leaf decomposition in a stream. Mycol. Prog. 3, 41–49 (2004).

  20. 20.

    Grossart, H.-P., Wurzbacher, C., James, T. Y. & Kagami, M. Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecol. 19, 28–38 (2016).

  21. 21.

    Gulis, V., Suberkropp, K. & Rosemond, A. D. Comparison of fungal activities on wood and leaf litter in unaltered and nutrient-enriched headwater streams. Appl. Environ. Microbiol. 74, 1094–1101 (2008).

  22. 22.

    Wurzbacher, C., Rösel, S., Rychla, A. & Grossart, H.-P. Importance of saprotrophic freshwater fungi for pollen degradation. PLOS ONE 9, e94643 (2014).

  23. 23.

    Frenken, T. et al. Integrating chytrid fungal parasites into plankton ecology: research gaps and needs. Environ. Microbiol. 19, 3802–3822 (2017).

  24. 24.

    Cunliffe, M., Hollingsworth, A., Bain, C. & Taylor, J. D. Algal polysaccharide utilisation by saprotrophic planktonic marine fungi. Fungal Ecol. 30, 135–138 (2017).

  25. 25.

    Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

  26. 26.

    Woyke, T. & Rubin, E. M. Searching for new branches on the tree of life. Science 346, 698–699 (2014).

  27. 27.

    Mukherjee, S. et al. 1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life. Nat. Biotechnol. 35, 676–683 (2017).

  28. 28.

    Mangot, J.-F. et al. Accessing the genomic information of unculturable oceanic picoeukaryotes by combining multiple single cells. Sci. Rep. 7, 41498 (2017).

  29. 29.

    Heeger, F. et al. Long-read DNA metabarcoding of ribosomal rRNA in the analysis of fungi from aquatic environments. Mol. Ecol. Resour. 18, 1500–1514 (2018).

  30. 30.

    Khomich, M., Davey, M. L., Kauserud, H., Rasconi, S. & Andersen, T. Fungal communities in Scandinavian lakes along a longitudinal gradient. Fungal Ecol. 27, 36–46 (2017).

  31. 31.

    Giner, C. R. et al. Environmental sequencing provides reasonable estimates of the relative abundance of specific picoeukaryotes. Appl. Environ. Microbiol. 82, 4757–4766 (2016).

  32. 32.

    Seto, K., Kagami, M. & Degawa, Y. Phylogenetic position of parasitic chytrids on diatoms: characterization of a novel clade in chytridiomycota. J. Eukaryot. Microbiol. 64, 383–393 (2017).

  33. 33.

    Van den Wyngaert, S., Rojas-Jimenez, K., Seto, K., Kagami, M. & Grossart, H.-P. Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. J. Eukaryot. Microbiol. 65, 870–881 (2018).

  34. 34.

    Reich, M. & Labes, A. How to boost marine fungal research: a first step towards a multidisciplinary approach by combining molecular fungal ecology and natural products chemistry. Mar. Genomics 36, 57–75 (2017).

  35. 35.

    Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).

  36. 36.

    Tedersoo, L., Tooming-Klunderud, A. & Anslan, S. PacBio metabarcoding of fungi and other eukaryotes: errors, biases and perspectives. New Phytol. 217, 1370–1385 (2018).

  37. 37.

    Liu, J., Wang, J., Gao, G., Bartlam, M. G. & Wang, Y. Distribution and diversity of fungi in freshwater sediments on a river catchment scale. Front. Microbiol. 6, 329 (2015).

  38. 38.

    Wang, X. et al. Distribution and diversity of planktonic fungi in the west pacific warm pool. PLOS ONE 9, e101523 (2014).

  39. 39.

    Tisthammer, K. H., Cobian, G. M. & Ahmend, A. S. Global biogeography of marine fungi is shaped by the environment. Fungal Ecol. 19, 39–46 (2015).

  40. 40.

    Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).

  41. 41.

    Duarte, S., Bärlocher, F., Pascoal, C. & Cassio, F. Biogeography of aquatic hyphomycetes: current knowledge and future perspectives. Fungal Ecol. 19, 169–181 (2016).

  42. 42.

    Monchy, S. et al. Exploring and quantifying fungal diversity in freshwater lake ecosystems using rDNA cloning/sequencing and SSU tag pyrosequencing. Environ. Microbiol. 13, 1433–1453 (2011).

  43. 43.

    Picard, K. T. Coastal marine habitats harbor novel early-diverging fungal diversity. Fungal Ecol. 25, 1–13 (2017).

  44. 44.

    Tedersoo, L., Bahram, M., Puusepp, R., Henrik Nilsson, R. & James, T. Y. Novel soil-inhabiting clades fill gaps in the fungal tree of life. Microbiome 5, 42 (2017).

  45. 45.

    Tedersoo, L. et al. High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers. 90, 135–159 (2018).

  46. 46.

    Wurzbacher, C. et al. Introducing ribosomal tandem repeat barcoding for fungi. Mol. Ecol. Resour. 19, 118–127 (2018).

  47. 47.

    Jones, E. B. G., Hyde, K. D. & Pang, K.-L. (eds) Freshwater Fungi: and Fungal-like Organisms (De Gruyter, 2014).

  48. 48.

    Comeau, A. M., Vincent, W. F., Bernier, L. & Lovejoy, C. Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci. Rep. 6, 30120 (2016).

  49. 49.

    Hassett, B. T., Ducluzeau, A. L., Collins, R. E. & Gradinger, R. Spatial distribution of aquatic marine fungi across the western Arctic and sub-arctic. Environ. Microbiol. 19, 475–484 (2017).

  50. 50.

    Rojas-Jimenez, K. et al. Early diverging lineages within Cryptomycota and Chytridiomycota dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys, Antarctica. Sci. Rep. 7, e15348 (2017).

  51. 51.

    Braun, A. Über Chytridium: eine Gattung einzelliger Schmarotzergewächse auf Algen und Infusorien [German] (Königl Akademie der Wissenschaften, 1856).

  52. 52.

    Sparrow, F. K. Aguatic Phycomycetes (Michigan Univ. Press, 1960).

  53. 53.

    Ingold, T. C. An lllustrated Guide to Aquatic Hyphomycetes Vol. 30 (Freshwater Biological Association, 1975).

  54. 54.

    Bärlocher, F. in The Ecology of Aquatic Hyphomycetes (ed. Bärlocher, F.) 1–15 (Spinger, Heidelberg, 1992).

  55. 55.

    Chauvet, E., Cornut, J., Sridhar, K. R., Selosse, M.-A. & Bärlocher, F. Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecol. 19, 112–127 (2016).

  56. 56.

    Roth, F. J. Jr, Orpurt, P. A. & Ahearn, D. G. Occurrence and distribution of fungi in a subtropical marine environment. Can. J. Bot. 42, 375–383 (1964).

  57. 57.

    Raghukumar, C., Damare, S. R. & Singh, P. A review on deep-sea fungi: occurrence, diversity and adaptations. Botanica Marina 53, 479–492 (2010).

  58. 58.

    Nagano, Y. & Nagahama, T. Fungal diversity in deep-sea extreme environments. Fungal Ecol. 5, 463–471 (2012).

  59. 59.

    Zhang, X., Tang, G., Xu, X. Y., Nong, X. H. & Qi, S. H. Insights into deep-sea sediment fungal communities from the East Indian Ocean using targeted environmental sequencing combined with traditional cultivation. PLOS ONE 9, e109118 (2014).

  60. 60.

    Xu, W., Luo, Z.-H., Guo, S. & Pang, K.-L. Fungal community analysis in the deep-sea sediments of the Pacific Ocean assessed by comparison of ITS, 18S and 28S ribosomal DNA regions. Deep Sea Res. Part I Oceanogr. Res. Pap. 109, 51–60 (2016).

  61. 61.

    Edgcomb, V. P., Beaudoin, D., Gast, R., Biddle, J. F. & Teske, A. Marine subsurface eukaryotes: the fungal majority. Environ. Microbiol. 13, 172–183 (2011).

  62. 62.

    Ivarsson, M., Bengtson, S. & Neubeck, A. The igneous oceanic crust–Earth’s largest fungal habitat? Fungal Ecol. 20, 249–255 (2016).

  63. 63.

    Orsi, W., Biddle, J. F. & Edgcomb, V. Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLOS ONE 8, e56335 (2013).

  64. 64.

    López-García, P., Vereshchaka, A. & Moreira, D. Eukaryotic diversity associated with carbonates and fluid–seawater interface in Lost City hydrothermal field. Environ. Microbiol. 9, 546–554 (2007).

  65. 65.

    Connell, L., Barrett, A., Templeton, A. & Staudigel, H. Fungal diversity associated with an active deep sea volcano: Vailulu’u Seamount, Samoa. Geomicrobiol. J. 26, 597–605 (2009).

  66. 66.

    Le Calvez, T., Burgaud, G., Mahé, S., Barbier, G. & Vandenkoornhuyse, P. Fungal diversity in deep-sea hydrothermal ecosystems. Appl. Environ. Microbiol. 75, 6415–6421 (2009).

  67. 67.

    Kutty, S. N. & Philip, R. Marine yeasts — a review. Yeast 25, 465–483 (2008).

  68. 68.

    Li, L., Singh, P., Liu, Y., Pan, S. & Wang, G. Diversity and biochemical features of culturable fungi from the coastal waters of Southern China. AMB Express 4, 60 (2014).

  69. 69.

    Comic, L., Rankovic, B., Novevska, V. & Ostojic, A. Diversity and dynamics of the fungal community in Lake Ohrid. Aquat. Biol. 9, 169–176 (2010).

  70. 70.

    Gonçalves, V. N., Vaz, A. B. M., Rosa, C. A. & Rosa, L. H. Diversity and distribution of fungal communities in lakes of Antarctica. FEMS Microbiol. Ecol. 82, 459–471 (2012).

  71. 71.

    Gunde-Cimerman, N. et al. Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity. Phys. Chem. Earth 28, 1273–1278 (2003).

  72. 72.

    Hoshino, T. et al. Antifreeze proteins from snow mold fungi. Can. J. Bot. 81, 1175–1181 (2003).

  73. 73.

    Miyamoto, T., Koda, K., Kawaguchi, A. & Uraki, Y. Ligninolytic activity at 0°C of fungi on oak leaves under snow cover in a mixed forest in Japan. Microb. Ecol. 74, 322–331 (2017).

  74. 74.

    Jones, E. B. G. & Pang, K. L. Tropical aquatic fungi. Biodivers. Conserv. 21, 2403–2423 (2012).

  75. 75.

    Zhang, T., Wang, N. F., Zhang, Y. Q., Liu, H. Y. & Yu, L. Y. Diversity and distribution of aquatic fungal communities in the Ny-Ålesund region, Svalbard (High Arctic). Microb. Ecol. 71, 543–554 (2016).

  76. 76.

    Nagano, Y. et al. Fungal diversity in deep-sea sediments associated with asphalt seeps at the Sao Paulo Plateau. Deep Sea Res. Part II Top. Stud. Oceanogr. 146, 59–67 (2017).

  77. 77.

    Sohlberg, E. et al. Revealing the unexplored fungal communities in deep groundwater of crystalline bedrock fracture zones in Olkiluoto, Finland. Front. Microbiol. 6, 573 (2015).

  78. 78.

    Nawaz, A. et al. Superimposed pristine limestone aquifers with marked hydrochemical differences exhibit distinct fungal communities. Front. Microbiol. 7, 666 (2016).

  79. 79.

    Nawaz, A. et al. First insights into the living groundwater mycobiome of the terrestrial biogeosphere. Water Res. 145, 50–61 (2018).

  80. 80.

    Brad, T., Braster, M., van Breukelen, B. M., van Straalen, N. M. & Rölinget, W. F. M. Eukaryotic diversity in an anaerobic aquifer polluted with landfill leachate. Appl. Environ. Microbiol. 74, 3959–3968 (2008).

  81. 81.

    Fasanella, C. C. et al. The selection exerted by oil contamination on mangrove fungal communities. Water Air Soil Pollut. 223, 4233–4243 (2012).

  82. 82.

    Simister, R. L. et al. Degradation of oil by fungi isolated from Gulf of Mexico beaches. Mar. Pollut. Bull. 100, 327–333 (2015).

  83. 83.

    Lepere, C., Boucher, D., Jardillier, L., Domaizon, I. & Debroas, D. Succession and regulation factors of small eukaryote community composition in a lacustrine ecosystem (Lake Pavin). Appl. Environ. Microbiol. 72, 2971–2981 (2006).

  84. 84.

    Jobard, M., Rasconi, S., Solinhac, L., Cauchie, H. M. & Sime-Ngando, T. Molecular and morphological diversity of fungi and the associated functions in three European nearby lakes. Environ. Microbiol. 14, 2480–2494 (2012).

  85. 85.

    Ishida, S., Nozaki, D., Grossart, H.-P. & Kagami, M. Novel basal, fungal lineages from freshwater phytoplankton and lake samples. Environ. Microbiol. Rep. 7, 435–441 (2015).

  86. 86.

    Panzer, K. et al. Identification of habitat-specific biomes of aquatic fungal communities using a comprehensive nearly full-length 18S rRNA dataset enriched with contextual data. PLOS ONE 10, e0134377 (2015).

  87. 87.

    Wurzbacher, C. et al. High habitat-specificity in fungal communities in oligo-mesotrophic, temperate Lake Stechlin (North-East Germany). MycoKeys 16, 17–44 (2016).

  88. 88.

    Lazarus, K. L. & James, T. Y. Surveying the biodiversity of the Cryptomycota using a targeted PCR approach. Fungal Ecol. 14, 62–70 (2015).

  89. 89.

    Jeffries, T. C. et al. Partitioning of fungal assemblages across different marine habitats. Environ. Microbiol. Rep. 8, 235–238 (2016).

  90. 90.

    Wang, Y. et al. Distinct seasonality of chytrid-dominated benthic fungal communities in the neritic oceans (Bohai Sea and North Yellow Sea). Fungal Ecol. 30, 55–66 (2017).

  91. 91.

    Naff, C. S., Darcy, J. L. & Schmidt, S. K. Phylogeny and biogeography of an uncultured clade of snow chytrids. Environ. Microbiol. 15, 2672–2680 (2013).

  92. 92.

    Hassett, B. T. & Gradinger, R. Chytrids dominate arctic marine fungal communities. Environ. Microbiol. 18, 2001–2009 (2016).

  93. 93.

    Rämä, T., Hassett, B. T. & Bubnova, E. Arctic marine fungi: from filaments and flagella to operational taxonomic units and beyond. Botanica Marina 60, 433–452 (2017).

  94. 94.

    Gilbert, J. A. & Stephens, B. Microbiology of the built environment. Nat. Rev. Microbiol. 16, 661–670 (2018).

  95. 95.

    Babič, M. N., Zalar, P., Ženko, B., Džeroski, S. & Gunde-Cimerman, N. Yeasts and yeast-like fungi in tap water and groundwater, and their transmission to household appliances. Fungal Ecol. 20, 30–39 (2016).

  96. 96.

    Hervé, V., Leroy, B., Pires, A. D. S. & Lopez, P. J. Aquatic urban ecology at the scale of a capital: community structure and interactions in street gutters. ISME J. 12, 253–266 (2017).

  97. 97.

    Becker, J. G. & Shaw, C. G. Fungi in domestic sewage-treatment plants. Appl. Microbiol. 3, 173–180 (1955).

  98. 98.

    Evans, T. N. & Seviour, R. J. Estimating biodiversity of fungi in activated sludge communities using culture-independent methods. Microb. Ecol. 63, 773–786 (2012).

  99. 99.

    Chouari, R. et al. Eukaryotic molecular diversity at different steps of the wastewater treatment plant process reveals more phylogenetic novel lineages. World J. Microbiol. Biotechnol. 33, 44 (2017).

  100. 100.

    Hirakata, Y., Hatamoto, M., Oshiki, M., Araki, N. & Yamaguchi, T. in Frontiers International Conference on Wastewater Treatment and Modelling (ed. Mannina, G.) 218–224 (Springer International Publishing, 2017).

  101. 101.

    Miyaoka, Y., Hatamoto, M., Yamaguchi, T. & Syutsubo, K. Eukaryotic community shift in response to organic loading rate of an aerobic trickling filter (down-flow hanging sponge reactor) treating domestic sewage. Microb. Ecol. 73, 801–814 (2017).

  102. 102.

    Maza-Márquez, P. et al. Community structure, population dynamics and diversity of fungi in a full-scale membrane bioreactor (MBR) for urban wastewater treatment. Water Res. 105, 507–519 (2016).

  103. 103.

    Hofmann, U. et al. Evaluation of the applicability of the aquatic ascomycete Phoma sp. UHH 5-1-03 for the removal of pharmaceutically active compounds from municipal wastewaters using membrane bioreactors. Eng. Life Sci. 18, 510–519 (2018).

  104. 104.

    Seppälä, S., Knop, D., Solomon, K. V. & O’Malley, M. A. The importance of sourcing enzymes from non-conventional fungi for metabolic engineering and biomass breakdown. Metab. Eng. 44, 45–59 (2017).

  105. 105.

    Zhou, W. et al. Novel fungal pelletization-assisted technology for algae harvesting and wastewater treatment. Appl. Biochem. Biotechnol. 167, 214–228 (2012).

  106. 106.

    Letcher, P. M. et al. Characterization of amoeboaphelidium protococcarum, an algal parasite new to the cryptomycota isolated from an outdoor algal pond used for the production of biofuel. PLOS ONE 8, e56232 (2013).

  107. 107.

    Beyter, D. et al. Diversity, productivity and stability of an industrial microbial ecosystem. Appl. Environ. Microbiol. 82, 2494–2505 (2016).

  108. 108.

    Shurin, J. B. et al. Industrial-strength ecology: trade-offs and opportunities in algal biofuel production. Ecol. Lett. 16, 1393–1404 (2013).

  109. 109.

    Carney, L. T. & Lane, T. W. Parasites in algae mass culture. Front. Microbiol. 5, 278 (2014).

  110. 110.

    Letcher, P. M. et al. Morphological, molecular, and ultrastructural characterization of Rozella rhizoclosmatii, a new species in Cryptomycota. Fungal Biol. 121, 1–10 (2017).

  111. 111.

    Lightner, D. V. & Redman, R. M. Shrimp diseases and current diagnostic methods. Aquaculture 164, 201–220 (1998).

  112. 112.

    Nylund, S., Nylund, A., Watanabe, K., Arnesen, C. E. & Karlsbakk, E. Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the salmon louse (Lepeophtheirus salmonis, Copepoda) and Atlantic salmon (Salmo salar). J. Eukaryot. Microbiol. 57, 95–114 (2010).

  113. 113.

    Bartelme, R. P., Oyserman, B. O., Blom, J. E., Sepulveda-Villet, O. J. & Newton, R. J. Stripping away the soil: plant growth promoting microbiology opportunities in aquaponics. Front. Microbiol. 9, 8 (2018).

  114. 114.

    Nobu, M. K. et al. Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor. ISME J. 9, 1710–1722 (2015).

  115. 115.

    Zhdanova, N. N., Zakharchenko, V. A., Vember, V. V. & Nakonechnaya, L. T. Fungi from Chernobyl: mycobiota of the inner regions of the containment structures of the damaged nuclear reactor. Mycol. Res. 104, 1421–1426 (2000).

  116. 116.

    Neu, L. et al. Ugly ducklings-the dark side of plastic materials in contact with potable water. NPJ Biofilms Microbiomes 4, 7 (2018).

  117. 117.

    Kettner, M. T., Rojas-Jimenez, K., Oberbeckmann, S., Labrenz, M. & Grossart, H.-P. Microplastics alter composition of fungal communities in aquatic ecosystems. Environ. Microbiol. 19, 4447–4459 (2017).

  118. 118.

    Arias-Andres, M., Klümper, U., Rojas-Jimenez, K. & Grossart, H.-P. Microplastic pollution increases gene exchange in aquatic ecosystems. Environ. Pollut. 237, 253–261 (2018).

  119. 119.

    Herrero, N., Sánchez Márquez, S. & Zabalgogeazcoa, I. Mycoviruses are common among different species of endophytic fungi of grasses. Arch. Virol. 154, 327–330 (2009).

  120. 120.

    Nerva, L. et al. Multiple approaches for the detection and characterization of viral and plasmid symbionts from a collection of marine fungi. Virus Res. 219, 22–38 (2016).

  121. 121.

    Gulis, V. & Suberkropp, K. Interactions between stream fungi and bacteria associated with decomposing leaf litter at different levels of nutrient availability. Aquat. Microb. Ecol. 30, 149–157 (2003).

  122. 122.

    Park, S. T., Collingwood, A. M., St-Hilaire, S. & Sheridan, P. P. Inhibition of batrachochytrium dendrobatidis caused by bacteria isolated from the skin of Boreal toads, Anaxyrus (Bufo) boreas boreas, from Grand Teton National Park, WY, USA. Microbiol. Insights 7, 1–8 (2014).

  123. 123.

    Mille-Lindblom, C. & Tranvik, L. J. Antagonism between bacteria and fungi on decomposing aquatic plant litter. Microb. Ecol. 45, 173–182 (2003).

  124. 124.

    Schorn, S. & Cypionka, H. A. Crispy diet: grazers of achromatium oxaliferum in Lake Stechlin sediments. Microb. Ecol. 76, 584–587 (2018).

  125. 125.

    Bengtsson, G. Interactions between fungi, bacteria and beech leaves in a stream microcosm. Oecologia 89, 542–549 (1992).

  126. 126.

    Senga, M., Yabe, S., Nakamura, T. & Kagami, M. Influence of parasitic chytrids on the quantity and quality of algal dissolved organic matter (AOM). Water Res. 145, 346–353 (2018).

  127. 127.

    Deveau, A. et al. Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol. Rev. 42, 335–352 (2018).

  128. 128.

    Corsaro, D. et al. New insights from molecular phylogenetics of amoebophagous fungi (Zoopagomycota, Zoopagales). Parasitol. Res. 117, 157–167 (2018).

  129. 129.

    Canter-Lund, H. & Lund, J. W. G. Freshwater Algae: their Microscopic World Explored (Biopress Ltd, Bristol, UK,1995).

  130. 130.

    Lee, S. S., Ha, J. K. & Cheng, K. J. Relative contributions of bacteria, protozoa, and fungi to in vitro degradation of orchard grass cell walls and their interactions. Appl. Environ. Microbiol. 66, 3807–3813 (2000).

  131. 131.

    Lueders, T., Wagner, B., Claus, P. & Friedrich, M. W. Stable isotope probing of rRNA and DNA reveals a dynamic methylotroph community and trophic interactions with fungi and protozoa in oxic rice field soil. Environ. Microbiol. 6, 60–72 (2004).

  132. 132.

    Song, C. et al. Molecular and chemical dialogues in bacteria-protozoa interactions. Sci. Rep. 5, 12837 (2015).

  133. 133.

    Gleason, F. H., Marano, A. V., Lilje, O. & Lange, L. What has happened to the “aquatic phycomycetes” (sensu Sparrow)? Part I: a brief historical perspective. Fungal Biol. Rev. 32, 26–33 (2018).

  134. 134.

    Raghukumar, C. in Seaweed Taxonomic Identification, Aquaculture, Resource Environment, Fouling and Disease (ed. Tewari, A.) 366–385 (Central Salt and Marine Chemicals Research Institute, 2006).

  135. 135.

    Canter, H. M. & Lund, J. W. G. The parasitism of planktonic desmids by fungi. Österreichische Bot. Zeitschrift 116, 351–377 (1969).

  136. 136.

    Hanic, L., Sekimoto, A. S. & Bates, S. S. Oomycete and chytrid infections of the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae) from Prince Edward Island, Canada. Botany 87, 1096–1105 (2009).

  137. 137.

    Czeczuga, B., Godlewska, A. & Kozłowska, M. Zoosporic fungi growing on the carapaces of dead zooplankton organisms. Limnologica 30, 37–43 (2000).

  138. 138.

    Willsey, T., Chatterton, S. & Cárcamo, H. Interactions of root-feeding insects with fungal and oomycete plant pathogens. Front. Plant Sci. 8, 1764 (2017).

  139. 139.

    Picard, K. T., Letcher, P. M. & Powell, M. J. Evidence for a facultative mutualist nutritional relationship between the green coccoid alga Bracteacoccus sp.(Chlorophyceae) and the zoosporic fungus Rhizidium phycophilum (Chytridiomycota). Fungal. Biol. 117, 319–328 (2013).

  140. 140.

    Allen, J. L. et al. Allelopathic inhibition of primary producer growth and photosynthesis by aquatic fungi. Fungal Ecol. 29, 133–138 (2017).

  141. 141.

    Hawksworth, D. L. in Aquatic Mycology across the Millennium (eds Hyde, K. D., Ho, W. & Pointing, S. B.) 1–7 (Fungal Diversity Press, 2000).

  142. 142.

    Hom, E. F. Y. & Murray, A. W. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345, 94 (2014).

  143. 143.

    Gomes, F. C. et al. The diversity and extracellular enzymatic activities of yeasts isolated from water tanks of Vriesea minarum, an endangered bromeliad species in Brazil, and the description of Occultifur brasiliensis fa, sp. nov. Antonie Van Leeuwenhoek 107, 597–611 (2015).

  144. 144.

    Marins, J. F. D. & Carrenho, R. Arbuscular mycorrhizal fungi and dark septate fungi in plants associated with aquatic environments. Acta Bot. Brasil. 31, 295–308 (2017).

  145. 145.

    Suryanarayanan, T. S., Kumaresan, V. & Johnson, J. A. Foliar fungal endophytes from two species of the mangrove Rhizophora. Can. J. Microbiol. 44, 1003–1006 (1998).

  146. 146.

    Viterbo, A. & Horwitz, B. in Cellular and Molecular Biology of Filamentous Fungi (eds Borkovich, K. & Ebbole, D.) 676–693 (ASM Press, Washington, 2010).

  147. 147.

    Letcher, P. M. Morphology, ultrastructure, and molecular phylogeny of Rozella multimorpha, a new species in cryptomycota. J. Eukaryot. Microbiol. 65, 180–190 (2018).

  148. 148.

    Howe, M. J. & Suberkropp, K. Effects of mycoparasitism on an aquatic hyphomycete growing on leaf litter. Mycologia 85, 898–901 (1993).

  149. 149.

    Skerratt, L. F. et al. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4, 125 (2007).

  150. 150.

    Ebert, D. Ecology, Epidemiology, and Evolution of Parasitism in Daphnia (National Center for Biotechnology Information, Bethesda (MD), US, 2005).

  151. 151.

    Johnson, P. T. J., Ives, A. R., Lathrop, R. C. & Carpenter, S. R. Long-term disease dynamics in lakes: causes and consequences of chytrid infections in Daphnia populations. Ecology 90, 132–144 (2009).

  152. 152.

    Yarden, O. Fungal association with sessile marine invertebrates. Front. Microbiol. 5, 228–228 (2014).

  153. 153.

    Whisler, H. C., Zebold, S. L. & Shemanchuk, J. A. Life history of Coelomomyces psorophorae. Proc. Natl Acad. Sci. USA 72, 693–696 (1975).

  154. 154.

    Kagami, M., von Elert, E., Ibelings, B. W., de Bruin, A. & Van Donk, E. The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proc. Biol. Sci. 274, 1561–1566 (2007).

  155. 155.

    Schmeller, D. S. et al. Microscopic aquatic predators strongly affect infection dynamics of a globally emerged pathogen. Curr. Biol. 24, 176–180 (2014).

  156. 156.

    McCreadie, J. W., Adler, P. H. & Beard, C. E. Ecology of symbiotes of larval black flies (diptera: simuliidae): distribution, diversity, and scale. Environ. Entomol. 40, 289–302 (2011).

  157. 157.

    Lichtwardt, R. W. The Trichomycetes: Fungal Associates of Arthropods (Springer-Verlag, NY, 1986).

  158. 158.

    Wijayawardene, N. N. et al. Notes for genera: basal clades of Fungi (including Aphelidiomycota, Basidiobolomycota, Blastocladiomycota, Calcarisporiellomycota, Caulochytriomycota, Chytridiomycota, Entomophthoromycota, Glomeromycota, Kickxellomycota, Monoblepharomycota, Mortierellomycota, Mucoromycota, Neocallimastigomycota, Olpidiomycota, Rozellomycota and Zoopagomycota). Fungal Divers. 92, 43–129 (2018).

  159. 159.

    Paterson, R. A. Observations on two species of Rhizophydium from Northern Michigan. Mycol. Res. 46, 530–536 (1963).

  160. 160.

    Chamberlain, S. A., Bronstein, J. L. & Rudgers, J. A. How context dependent are species interactions? Ecol. Lett. 17, 881–890 (2014).

  161. 161.

    Thompson, J. N. The Geographic Mosaic of Coevolution (Chicago Univ. Press, 2005).

  162. 162.

    Anderson, J. L. & Shearer, C. A. Population genetics of the aquatic fungus tetracladium marchalianum over space and time. PLOS ONE 6, e15908 (2011).

  163. 163.

    Gleason, F. H. et al. Ecological functions of zoosporic hyperparasites. Front. Microbiol. 5, 244 (2014).

  164. 164.

    Parratt, S. R. & Laine, A.-L. The role of hyperparasitism in microbial pathogen ecology and evolution. ISME J. 10, 1815–1822 (2016).

  165. 165.

    Lefèvre, E., Letcher, P. M. & Powell, M. J. Temporal variation of the small eukaryotic community in two freshwater lakes: emphasis on zoosporic fungi. Aquat. Microb. Ecol. 67, 91–105 (2012).

  166. 166.

    Lepelletier, F. et al. Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomycetaceae fam. nov.), a chytrid infecting marine dinoflagellates. Protist 165, 230–244 (2014).

  167. 167.

    Gutiérrez, D. et al. Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Appl. Environ. Microbiol. 78, 8547–8554 (2012).

  168. 168.

    Gleason, F. H., Kagami, M., Lefèvre, E. & Sime-Ngando, T. The ecology of chytrids in aquatic ecosystems: roles in food web dynamics. Fungal Biol. Rev. 22, 17–25 (2008).

  169. 169.

    Sime-Ngando, T. Phytoplankton chytridiomycosis: fungal parasites of phytoplankton and their imprints on the food web dynamics. Front. Microbiol. 12, 361 (2012).

  170. 170.

    Gachon, C. M. M., Sime-Ngando, T., Strittmatter, M., Chambouvet, A. & Kim, G. H. Algal diseases: spotlight on a black box. Trends Plant Sci. 15, 633–640 (2010).

  171. 171.

    Harms, H., Schlosser, D. & Wick, L. Y. Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat. Rev. Microbiol. 9, 177–192 (2011).

  172. 172.

    Suberkropp, K. & Klug, M. J. The maceration of deciduous leaf litter by aquatic hyphomycetes. Can. J. Bot. 58, 1025–1031 (1980).

  173. 173.

    Crowther, T. W. & Grossart, H.-P. in Trophic Ecology: Bottom-Up and Top-Down Interactions Across Aquatic and Terrestrial Systems (eds Hanley, T. C. & La Pierre, K. J.) 260–287 (Cambridge Univ. Press, 2015).

  174. 174.

    Grami, B. et al. Functional effects of parasites on food web properties during the spring diatom bloom in Lake Pavin: a linear inverse modeling analysis. PLOS ONE 6, e23273 (2011).

  175. 175.

    Bochdansky, A. B., Clouse, M. A. & Herndl, G. J. Eukaryotic microbes, principally fungi and labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J. 11, 362–373 (2017).

  176. 176.

    Scholz, B., Küpper, F. C., Vyverman, W. & Karsten, U. Eukaryotic pathogens (Chytridiomycota and Oomycota) infecting marine microphytobenthic diatoms–a methodological comparison. J. Phycol. 50, 1009–1019 (2014).

  177. 177.

    Attermeyer, K., Premke, K., Hornick, T., Hilt, S. & Grossart, H.-P. Ecosystem-level studies of terrestrial carbon reveal contrasting bacterial metabolism in different aquatic habitats. Ecology 94, 2754–2766 (2013).

  178. 178.

    Brouard, O. et al. Understorey environments influence functional diversity in tank-bromeliad ecosystems. Freshw. Biol. 57, 815–823 (2012).

  179. 179.

    Dethier, M. N. Degrading detritus: changes in food quality of aging kelp tissue varies with species. J. Exp. Mar. Biol. Ecol. 460, 72–79 (2014).

  180. 180.

    Raja, H. A., Shearer, C. A. & Tsui, C. K.-M. Freshwater fungi. eLS https://doi.org/10.1002/9780470015902.a0027210 (2018).

  181. 181.

    Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R. & Cushing, C. E. The river continuum concept. Can. J. Fish. Aquat. Sci. 37, 130–137 (1980).

  182. 182.

    Biswas, S. & Wagner, H. Landscape contrast: a solution to hidden assumptions in the metacommunity concept? Landscape Ecol. 27, 621–631 (2012).

  183. 183.

    Battin, T. J., Wille, A., Psenner, R. & Richter, A. Large-scale environmental controls on microbial biofilms in high-alpine streams. Biogeosciences 1, 159–171 (2004).

  184. 184.

    Ortiz-Álvarez, R., Triadó-Margarit, X., Camarero, L., Casamayor, E. O. & Catalan, J. High planktonic diversity in mountain lakes contains similar contributions of autotrophic, heterotrophic and parasitic eukaryotic life forms. Sci. Rep. 8, 4457 (2018).

  185. 185.

    Miura, A. & Urabe, J. Changes in epilithic fungal communities under different light conditions in a river: a field experimental study. Limnol. Oceanogr. 62, 579–591 (2017).

  186. 186.

    Fabian, J. et al. Environmental control on microbial turnover of leaf carbon in streams – ecological function of phototrophic-heterotrophic interactions. Front. Microbiol. 9, 1044 (2018).

  187. 187.

    Mohamed, D. J. & Martiny, J. B. H. Patterns of fungal diversity and composition along a salinity gradient. ISME J. 5, 379–388 (2011).

  188. 188.

    Junk, W. J., Bayley, P. B. & Sparks, R. E. in Proceedings of the International Large River Symposium (LARS) (ed. Dodge, D. P.) 110–127 (Canadian Special Publication of Fisheries and Aquatic Sciences, 1989).

  189. 189.

    Cole, J. J. et al. Differential support of lake food webs by three types of terrestrial organic carbon. Ecol. Lett. 9, 558–568 (2006).

  190. 190.

    Rösel, S., Rychla, A., Wurzbacher, C. & Grossart, H.-P. Effects of pollen leaching and microbial degradation on organic carbon and nutrient availability in lake water. Aquat. Sci. 74, 87–99 (2012).

  191. 191.

    Sommer, U. et al. Beyond the Plankton Ecology Group (PEG) model: mechanisms driving plankton succession. Annu. Rev. Ecol. Evol. Syst. 43, 429–448 (2012).

  192. 192.

    Truong, C. et al. How to know the fungi: combining field inventories and DNA-barcoding to document fungal diversity. New Phytol. 214, 913–919 (2017).

  193. 193.

    Tkacz, A., Hortala, M. & Poole, P. S. Absolute quantitation of microbiota abundance in environmental samples. Microbiome 6, 110 (2018).

  194. 194.

    West, P. T., Probst, A., Grigoriev, I. V., Thomas, B. C. & Banfield, J. F. Genome-reconstruction for eukaryotes from complex natural microbial communities. Genome Res. 28, 569–580 (2018).

  195. 195.

    Ahrendt, S. R. et al. Leveraging single-cell genomics to expand the fungal tree of life. Nat. Microbiol. 3, 1417–1428 (2018).

  196. 196.

    Garcia, S. L. et al. Model communities hint at promiscuous metabolic linkages between ubiquitous free-living freshwater bacteria. mSphere 3, e00202-18 (2018).

  197. 197.

    Mondo, S. J. et al. Widespread adenine N6-methylation of active genes in fungi. Nat. Genet. 49, 964–968 (2017).

  198. 198.

    Spatafora, J. W. et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108, 1028–1046 (2016).

  199. 199.

    Haag, K. L. et al. Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proc. Natl Acad. Sci. USA 111, 15480–15485 (2014).

  200. 200.

    Agha, R., Gross, A., Gerphagnon, M., Rohrlack, T. & Wolinska, J. Fitness and eco-physiological response of a chytrid fungal parasite infecting planktonic cyanobacteria to thermal and host genotype variation. Parasitology 145, 1279–1286 (2018).

  201. 201.

    Orsi, W. D. Ecology and evolution of seafloor and subseafloor microbial communities. Nat. Rev. Microbiol. 16, 671–683 (2018).

  202. 202.

    Wankel, S. D. et al. Evidence for fungal and chemodenitrification based N2O flux from nitrogen impacted coastal sediments. Nat. Commun. 8, 15595 (2017).

  203. 203.

    Drake, H. et al. Anaerobic consortia of fungi and sulfate reducing bacteria in deep granite fractures. Nat. Commun. 8, 55 (2017).

  204. 204.

    Jobard, M., Rasconi, S. & Sime-Ngando, T. Fluorescence in situ hybridization of uncultured zoosporic fungi: Testing with clone-FISH and application to freshwater samples using CARD-FISH. J. Microbiol. Methods 83, 236–243 (2010).

  205. 205.

    Karpov, S. A. et al. Monoblepharidomycetes diversity includes new parasitic and saprotrophic species with highly intronized rDNA. Fungal Biol. 121, 729–741 (2017).

  206. 206.

    Turchetti, B. et al. Psychrophilic yeasts from Antarctica and European glaciers: description of Glaciozyma gen. nov., Glaciozyma martinii sp. nov. and Glaciozyma watsonii sp. nov. Extremophiles 15, 573–586 (2011).

  207. 207.

    Frank, J. L., Coffan, R. A. & Southworth, D. Aquatic gilled mushrooms: Psathyrella fruiting in the Rogue River in southern Oregon. Mycologia 102, 93–107 (2010).

Download references

Acknowledgements

The authors thank J. Salazar for help designing the draft figures. H.P.G. was supported by Deutsche Forschungsgemeinschaft (DFG) grants GR1540/23-1 and GR1540/ 30–1, S.V.d.W. by DFG grant WY175/1-1 and M.C. by European Research Council (ERC) grant MYCO-CARB 772584. They thank the reviewers for their valuable comments and suggestions.

Reviewer information

Nature Reviews Microbiology thanks L. Tedersoo and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

  1. Department of Experimental Limnology, Leibniz Institute of Freshwater Ecology and Inland Fisheries, Stechlin, Germany

    • Hans-Peter Grossart
    •  & Silke Van den Wyngaert
  2. Institute of Biochemistry and Biology, Potsdam University, Potsdam, Germany

    • Hans-Peter Grossart
  3. Yokohama National University, Graduate School of Environment and Information Sciences, Hodogaya-ku, Yokohama, Kanagawa, Japan

    • Maiko Kagami
  4. Chair of Urban Water Systems Engineering, Technical University of Munich, Garching, Germany

    • Christian Wurzbacher
  5. Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, Devon, UK

    • Michael Cunliffe
  6. School of Biological and Marine Sciences, University of Plymouth, Drake Circus, Plymouth, Devon, UK

    • Michael Cunliffe
  7. Escuela de Biologia, Universidad de Costa Rica, San Pedro, San Jose, Costa Rica

    • Keilor Rojas-Jimenez

Authors

  1. Search for Hans-Peter Grossart in:

  2. Search for Silke Van den Wyngaert in:

  3. Search for Maiko Kagami in:

  4. Search for Christian Wurzbacher in:

  5. Search for Michael Cunliffe in:

  6. Search for Keilor Rojas-Jimenez in:

Contributions

H.P.G. researched data for the article. H.P.G., S.V.d.W., M.K., C.W., M.C. and K.R-J. wrote the article, contributed substantially to discussion of the content and reviewed and edited the manuscript before submission.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Hans-Peter Grossart.

Supplementary information

Glossary

Indwellers

Fungi that are well adapted and constantly active in aquatic habitats.

Periodic immigrants

Fungi that are less adapted to and only periodically active in aquatic habitats.

Versatile immigrants

Fungi that are little adapted to and only sporadically active in aquatic habitats.

Carbon pump

A mechanism whereby atmospheric carbon is sequestered by vertical transfer to deep waters and sediments.

Short-term disturbances

Pulsed event-based disturbances referring to strong single events such as storms and droughts.

Long-term anthropogenic disturbances

Gradually increasing press disturbances such as global climate change or urbanization, both leading to species loss and shifts in community composition.

Mycorrhiza

A fungus in symbiosis with a vascular plant via the root in the rhizosphere.

Mycoparasitism

Fungi parasitizing on other fungi.

Hyperparasites

Parasites of a host that is also a parasite.

Precursor rRNA

The precursor ribosomal RNA (rRNA) is a prespliced, full-length transcribed ribosomal operon including all functional and spacer regions.

About this article

Publication history

Published

DOI

https://doi.org/10.1038/s41579-019-0175-8