Abstract

Recent molecular evidence suggests a global distribution of marine fungi; however, the ecological relevance and corresponding biological contributions of fungi to marine ecosystems remains largely unknown. We assessed fungal biomass from the open Arctic Ocean by applying novel biomass conversion factors from cultured isolates to environmental sterol and CARD-FISH data. We found an average of 16.54 nmol m−3 of ergosterol in sea ice and seawater, which corresponds to 1.74 mg C m−3 (444.56 mg C m−2 in seawater). Using Chytridiomycota-specific probes, we observed free-living and particulate-attached cells that averaged 34.07 µg C m−3 in sea ice and seawater (11.66 mg C m−2 in seawater). Summed CARD-FISH and ergosterol values approximate 1.77 mg C m−3 in sea ice and seawater (456.23 mg C m−2 in seawater), which is similar to biomass estimates of other marine taxa generally considered integral to marine food webs and ecosystem processes. Using the GeoChip microarray, we detected evidence for fungal viruses within the Partitiviridae in sediment, as well as fungal genes involved in the degradation of biomass and the assimilation of nitrate. To bridge our observations of fungi on particulate and the detection of degradative genes, we germinated fungal conidia in zooplankton fecal pellets and germinated fungal conidia after 8 months incubation in sterile seawater. Ultimately, these data suggest that fungi could be as important in oceanic ecosystems as they are in freshwater environments.

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References

  1. 1.

    Berbee ML, James TY, Strullu-Derrien C. Early diverging fungi: diversity and impact at the dawn of terrestrial life. Annu Rev Microbiol. 2017;71:41–60.

  2. 2.

    Blackwell M. The fungi: 1, 2, 3…5.1 million species? Am J Bot. 2011;98:426–38.

  3. 3.

    Hawksworth DL, Lucking R. Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spectr. 2017. https://doi.org/10.1128/microbiolspec.FUNK-0052-2016.

  4. 4.

    Jones EBG, Suetrong S, Sakayaroj J, Bahkali AH, Abdel-Wahab MA, et al. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers. 2015;73:1–72.

  5. 5.

    Freeman KR, Martin AP, Karki D, Lynch RC, Mitter MS, Meyer AF, et al. Evidence that chytrids dominate fungal communities in high-elevation soils. Proc Natl Acad Sci USA. 2009;106:18315–20.

  6. 6.

    Comeau AM, Vincent WF, Bernier L, Lovejoy C. Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci Rep. 2016;6:30120.

  7. 7.

    Rojas-Jimenez K, Wurzbacher C, Bourne EC, Chiuchiolo A, Priscu JC, Grossard HPl. Early diverging lineages within Cryptomyocta and Chytridiomyocta dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys, Antarctica. Sci Rep. 2017;7:1.

  8. 8.

    Hassett BT, Gradinger R. Chytrids dominate Arctic marine fungal communities. Environ Microbiol. 2016;18:2001–9.

  9. 9.

    Bochdansky AB, Clouse MA, Herdl GJ. Eukaryotic microbes, principally fungi and Labyrinthulomycetes, dominate biomass on bathypelagic marine snow. ISME J. 2017;11:362–73.

  10. 10.

    Rämä T, Hassett BT, Bubnova E. Arctic marine fungi: from filaments and flagella to operational taxonomic units and beyond. Bot Mar. 2017;60:433–52.

  11. 11.

    Bluhm BA, Kosobokova KN, Carmack EC. A tale of two basins: an integrated physical and biological perspective of the deep Arctic Ocean. Prog Oceanogr. 2015;139:89–121.

  12. 12.

    Hansell DA, Kadko D, Bates NR. Degradation of terrigenous dissolved organic carbon in the Western Arctic Ocean. Sci. 2004;304:858–61.

  13. 13.

    Neff JC, Finlay JC, Zimov SA, Davydov SP, Carrasco JJ, Schuur EAG, et al. Seasonal changes in the age and structure of dissolved organic carbon in Siberian rivers and stream. Geophys Res Lett. 2006;33:L23401.

  14. 14.

    Dashtban M, Schraft H, Syed TA, Qin W. Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Bio. 2010;1:36–50.

  15. 15.

    Wotton RS, Malmqvist B. Feces in aquatic ecosystems: feeding animals transform organic matter into fecal pellets, which sink or are transported horizontally by currents; these fluxes relocate organic matter in aquatic ecosystems. Bioscience. 2001;51:537–44.

  16. 16.

    Turner JT. Zooplankton fecal pellets, marine snow, phytodetritus and the ocean’s biological pump. Prog Oceaogr. 2015;130:205–48.

  17. 17.

    Richardson MJ. Diversity and occurrence of coprophilous fungi. Mycol Res. 2001;105:387–402.

  18. 18.

    Hassett BT, Ducluzeau AL, Collins RE, Gradinger R. Spatial distribution of aquatic marine fungi across the western Arctic and sub-Arctic. Environ Microbiol. 2017;19:475–84.

  19. 19.

    Cleary AC, Soreide JE, Freese D, Neihoff B, Gabrielsen TM. Feeding by Calanus glacialis in a high arctic fjord: potential seasonal importance of alternative prey. ICES J Mar Sci. 2017;74:1937–46.

  20. 20.

    Zhang T, Wang NF, Zhang YQ, Liu HY, Yu LY. Diversity and distribution of fungal communities in the marine sediments of Kongfjorden, Svalbard (High Arctic). Sci Rep. 2015;5:14524.

  21. 21.

    Rämä T, Davey ML, Nordén J, Halvorsen R, Blaalid R, Mathiassen GH, et al. Fungi sailing the Arctic Ocean: speciose communities in North Atlantic driftwood as revealed by high-throughput amplicon sequencing. Microb Ecol. 2016;72:295–304.

  22. 22.

    Dupont S, Lemetais G, Ferreira T, Cayot P, Gervais P, Beney L. Ergosterol biosynthesis: a fungal pathway for life on land? Evolution. 2012;66:2961–8.

  23. 23.

    Weete JD, Abril M, Blackwell M. Phylogenetic distribution of fungal sterols. PLoS ONE. 2010;5:e10899.

  24. 24.

    Mille-Lindblom C, von Wachenfeldt E, Tranvik LJ. Ergosterol as a measure of living fungal biomass: persistence in environmental samples after fungal death. J Microbiol Methods. 2004;59:253–62.

  25. 25.

    Medina A, Probanza A, Gutierrez Manero FJ, Azcon R. Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant grwoth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Appl Soil Ecol. 2003;22:15–28.

  26. 26.

    Lee C, Howarth RW, Howes BL. Sterols in decomposing Spartina alterniflora and the use of ergosterol in estimating the contribution of fungi to detrital nitrogen. Limnol Oceanogr. 1980;25:290–303.

  27. 27.

    Newell SY. Fungal biomass and productivity. Method Microbiol. 2001;30:357–72.

  28. 28.

    Vernet M, Richardson TL, Metfies K, Nöthig EM, Peeken I. Models of plankton community changes during a warm water anomaly in Arctic waters show altered trophic pathways with minimal changes in carbon export. Front Mar Sci. 2017. https://doi.org/10.3389/fmars.2017.00160.

  29. 29.

    Stoeck T, Bass D, Nebel M, Christen R, Jones MDM, Breiner HW, et al. Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol. 2010;19:21–31.

  30. 30.

    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537–41.

  31. 31.

    Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.

  32. 32.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–D596.

  33. 33.

    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011;27:2194–2200.

  34. 34.

    Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhu kumar, et al. ARB: a software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71.

  35. 35.

    Pernthaler A, Pernthaler J, Amann R. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Envrion Microbiol. 2002;6:3094–101.

  36. 36.

    He Z, Gentry TJ, Schadt CW, Wu L, Liebich J, Chong SC, et al. GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J. 2007;1:67–77.

  37. 37.

    Van Nostrand JD, Yin H, He Z, Zhou J. Hybridization of environmental microbial community nucleic acids by GeoChip. Methods Mol Biol. 2016;1399:183–96.

  38. 38.

    Picard KT. Coastal marine habitats harbor novel early-diverging fungal diversity. Fungal Ecol. 2017;25:1–13.

  39. 39.

    Gessner MO, Chauvet E. Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol. 1993;59:502–7.

  40. 40.

    Maier MA, Peterson TD. Enumeration of parasitic chytrid zoospores in the Columbia River via quantitative PCR. Appl Environ Microbiol. 2016;82:3857–67.

  41. 41.

    Letcher PM, Vélez CG, Barrantes MA, Powell MJ, Churchill PF, Wakefield WS. Ultrastructural and molecular analyses of Rhizophydiales (Chytridiomycota) isolates from North America and Argentina. Mycol Res. 2008;112:759–82.

  42. 42.

    Karling JS. Brazilian chytrids. VI. Rhopalophlyctis and Chytriomyces, two new chitionphilic operculate genera. Am J Bot. 1945;32:362–9.

  43. 43.

    Lepelletier F, Karpov SA, Alacid E, Le Panse S, Bigeard E, Garcés E, et al. Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomycetaceae fam. nov.), a chytrid infecting marine dinoflagellates. Protist. 2014;165:230–44.

  44. 44.

    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. 2018;65:870–81.

  45. 45.

    Desmond E, Gribaldo S. Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukarotic feature. Genome Biol Evol. 2009;1:364–81.

  46. 46.

    Martin-Navarro CM, Lorenzo-Morales J, Machin RP, López-Arencibia A, Garcia-Castelleno JM, de Fuentes I, et al. Inhibition of 3-hydroxy-3-methylglutaryl-coenzyme A reductase and application of statins as a novel effective therapeutic approach against Acanthamoeba infections. Antimicrob Agents Chemother. 2013;57:375–81.

  47. 47.

    Brumfield KM, Laborde SM, Moroney JV. A model for the ergosterol biosynthetic pathway in Chlamydomonas reinhardtii. Eur J Phycol. 2017;52:64–74.

  48. 48.

    Najile SR, Molina MC, Ruiz-Trillo I, Uttaro AD. Sterol metabolism in the filasterean Capsaspora owczarzaki has features that resemble both fungi and animals. Open Biol. 2016;6:160029.

  49. 49.

    Sumathi JC, Raghukumar S, Kasbekar DP, Raghukumar C. Molecular evidence of fungal signatures in the marine protist Corallochytrium lamacisporum and its implications in the evolutions of animals and fungi. Protist. 2006;157:363–76.

  50. 50.

    Lepère C, Ostrowski M, Hartmann M, Zubkow MV, Scanlan DJ. In situ associations between marine photosynthetic picoeukaryotes and potential parasites—a role for fungi? Environ Microbiol Rep. 2016;8:445–51.

  51. 51.

    Reigstad M, Wexels Riser C, Wassmann P, Ratkova T. Vertical export of particulate organic carbon: attenuation, composition and loss rates in the northern Barents Sea. Deep-Sea Res Pt II. 2008;55:2308–19.

  52. 52.

    Gutiérrez MH, Pantoja S, Tejos E, Quiñones RA. The role of fungi in processing marine organic matter in the upwelling ecosystem off Chile. Mar Biol. 2011;158:205–19.

  53. 53.

    Wheeler PA, Gosselin M, Sherr E, Thibaultc D, Kirchman DL, Benner R, et al. Active cycling of organic carbon in the central Arctic Ocean. Nature. 1996;380:697–9.

  54. 54.

    Gradinger R. Sea ice algae: major contributors to primary production and algal biomass in the Chukchi and Beaufort Seas during May/June 2002. Deep-Sea Res Pt II. 2009;56:1201–12.

  55. 55.

    Auel H, Hagen W. Mesozooplankton community structure, abundance and biomass in the central Arctic Ocean. Mar Biol. 2002;140:1013–21.

  56. 56.

    Sherr EB, Sherr BF, Fessenden L. Heterotrophic protists in the central Arctic Ocean. Deep-Sea Res Pt II. 1997;44:1665–82.

  57. 57.

    Sherr EB, Sherr BF, Wheeler PA, Thompson K. Temporal and spatial variation in stocks of autotrophic and heterotrophic microbes in the upper water column of the central Arctic Ocean. Deep-Sea Res Pt I. 2003. https://doi.org/10.1016/S0967-0637(03)00031-1.

  58. 58.

    Terrado R, Medrinal E, Dasilva C, Thaler M, Vincent WF, Lovejoy C. Protist community composition during spring in an Arctic flaw lead polynya. Polar Biol. 2011;34:1901–14.

  59. 59.

    Taylor JD, Cunliffe M. Multi-year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J. 2016;10:2118–28.

  60. 60.

    Orsi W, Biddle FJ, Edgcomb V. Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLOS ONE 2013;8:e56335.

  61. 61.

    Ghabrial SA, Castrón JR, Jiang D, Nibert ML, Suzuki N. 50-plus years of fungal viruses. Virology. 2015;479:356–68.

  62. 62.

    Ortega-Arbulú A-S, Pichler M, Vuillemin A, Orsi WD. Effects of organic matter and low oxygen on the mycobenthos in a coastal lagoon. Environ Microbiol. 2018. https://doi.org/10.1111/1462-2920.14469.

  63. 63.

    Grebmeier JM, Barry JP. The influence of oceanographic processes on pelagic-benthic coupling in polar regions: a benthic perspective. J Mar Sci. 1991;2:495–518.

  64. 64.

    Jeffries TC, Curlevski NJ, Brown MV, Harrison DP, Doblin MA, Petrou K, et al. Partitioning of fungal assemblages across different marine habitats. Environ Microbiol Rep. 2016;8:235–8.

  65. 65.

    Sun JY, Song Y, Ma ZP, Zhang HJ, Yang ZD, Cai ZH, et al. Fungal community dynamics during a marine dioflagellate (Noctiluca scintillans) bloom. Mar Environ Res. 2017;131:183–94.

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Acknowledgements

We would like to acknowledge the funding support provided by UiT - the Arctic university of Norway and the Tromsø Research Foundation under the project Arctic SIZE, number 01VM/H15. We greatly acknowledge the support by the science team and the crew of the RV Polarstern and the grant support from AWI_PS106_00. We would like to thank Paul Dubourg and Roy Andres Lysa from the University of Tromsø for assistance with the CHN analyzer and with the flow cytometer, respectively, as well as Randi Olsen and Augusta Hlin Aspar Sundbø for assistance with laser scanning microscopy. We would like to acknowledge Céline Heuzé for generating CTD profiles and Thomas Isakeit from Texas A&M University for his spore trap. Analytical chemistry was supported by a United States Department of Agriculture's Agriculture and Food Research Initiative grant (2017-67013-26524). Sequencing data has been submitted to the NCBI SRA under BioBroject ID PRJNA449189, accession SAMN08888854–SAMN08888884. Microarray data have been archived in NCBI GEO, under accession GSE117831, GSM3309953–GSM3309954.

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  1. UiT Norges arktiske universitet, BFE, NFH bygget, Framstredet 6, 9019, Tromsø, Norway

    • B. T Hassett
    • , T. R. Vonnahme
    • , T. Rämä
    •  & R. Gradinger
  2. Texas A&M University, 435 Nagle Street, 2132 TAMU, College Station, TX, 77833, USA

    • E. J. Borrego
    •  & M. V. Kolomiets

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Correspondence to B. T Hassett.

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https://doi.org/10.1038/s41396-019-0368-1