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Microbial Ecology

, Volume 72, Issue 2, pp 295–304 | Cite as

Fungi Sailing the Arctic Ocean: Speciose Communities in North Atlantic Driftwood as Revealed by High-Throughput Amplicon Sequencing

  • Teppo Rämä
  • Marie L. Davey
  • Jenni Nordén
  • Rune Halvorsen
  • Rakel Blaalid
  • Geir H. Mathiassen
  • Inger G. Alsos
  • Håvard Kauserud
Fungal Microbiology

Abstract

High amounts of driftwood sail across the oceans and provide habitat for organisms tolerating the rough and saline environment. Fungi have adapted to the extremely cold and saline conditions which driftwood faces in the high north. For the first time, we applied high-throughput sequencing to fungi residing in driftwood to reveal their taxonomic richness, community composition, and ecology in the North Atlantic. Using pyrosequencing of ITS2 amplicons obtained from 49 marine logs, we found 807 fungal operational taxonomic units (OTUs) based on clustering at 97 % sequence similarity cut-off level. The phylum Ascomycota comprised 74 % of the OTUs and 20 % belonged to Basidiomycota. The richness of basidiomycetes decreased with prolonged submersion in the sea, supporting the general view of ascomycetes being more extremotolerant. However, more than one fourth of the fungal OTUs remained unassigned to any fungal class, emphasising the need for better DNA reference data from the marine habitat. Different fungal communities were detected in coniferous and deciduous logs. Our results highlight that driftwood hosts a considerably higher fungal diversity than currently known. The driftwood fungal community is not a terrestrial relic but a speciose assemblage of fungi adapted to the stressful marine environment and different kinds of wooden substrates found in it.

Keywords

454 sequencing Metabarcoding Marine fungi Marine wooden substrates Diversity Community ecology Biosystematics 

Notes

Acknowledgements

The Norwegian marine biobank, Marbank, provided logistic support and University of Tromsø the Arctic University of Norway and University of Oslo financial support. Rahman Mankettikkara kindly provided temperature and salinity data, Michael Greenacre statistical advice. Analyses were partly run on the Lifeportal and the Abel Cluster (http://www.uio.no/english/services/it/research/hpc/) at the University of Oslo.

Compliance with Ethical Standard

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2016_778_MOESM1_ESM.pdf (454 kb)
Fig. S1 Occurrence of the 50 most frequent OTUs in the 44 logs included in the community analysis (PDF 453 kb)
248_2016_778_MOESM2_ESM.pdf (196 kb)
Table S1 Explanatory variables recorded for the driftwood logs, their explanation and statistical properties (PDF 195 kb)
248_2016_778_MOESM3_ESM.xlsx (18 kb)
Table S2 Measured values of explanatory variables for the 44 logs included in the community analyses (XLSX 18 kb)
248_2016_778_MOESM4_ESM.xlsx (81 kb)
Table S3 OTU matrix used in the community analyses (XLSX 81 kb)
248_2016_778_MOESM5_ESM.xlsx (138 kb)
Table S4 OTU identities (XLSX 138 kb)
248_2016_778_MOESM6_ESM.pdf (281 kb)
Table S5 Generalised linear modelling (GLM) analyses of fungal group richness in driftwood logs (PDF 281 kb)
248_2016_778_MOESM7_ESM.docx (17 kb)
Table S6 Relationships between global nonmetric multidimensional scaling (GNMDS) ordination axes for fungal communities in 44 driftwood logs and explanatory variables (DOCX 16 kb)
248_2016_778_MOESM8_ESM.docx (160 kb)
Appendix S1 Supplementary methods (DOCX 159 kb)

References

  1. 1.
    Eriksson K-EL, Blanchette R, Ander P (1990) Microbial and enzymatic degradation of wood and wood components. Springer, GermanyCrossRefGoogle Scholar
  2. 2.
    Häggblom A (1982) Driftwood in Svalbard as an indicator of sea ice conditions. Geogr Ann A 64(1–2):81–94. doi: 10.2307/520496 CrossRefGoogle Scholar
  3. 3.
    Johansen S, Hytteborn H (2001) A contribution to the discussion of biota dispersal with drift ice and driftwood in the North Atlantic. J Biogeogr 28(1):105–115. doi: 10.1046/j.1365-2699.2001.00532.x CrossRefGoogle Scholar
  4. 4.
    Eggertsson Ó (1994) Driftwood as an indicator of relative changes in the influx of Arctic and Atlantic water into the coastal areas of Svalbard. Polar Res 13(2):209–218. doi: 10.3402/polar.v13i2.6694 CrossRefGoogle Scholar
  5. 5.
    Coûteaux M-M, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 10(2):63–66. doi: 10.1016/S0169-5347(00)88978-8 CrossRefPubMedGoogle Scholar
  6. 6.
    Jennings DH (1983) Some aspects of the physiology and biochemistry of marine fungi. Biol Rev 58(3):423–459. doi: 10.1111/j.1469-185X.1983.tb00395.x CrossRefGoogle Scholar
  7. 7.
    Blomberg A, Adler L (1992) Physiology of osmotolerance in fungi. Adv Microb Physiol 33:145–212. doi: 10.1016/S0065-2911(08)60217-9 CrossRefPubMedGoogle Scholar
  8. 8.
    Johnson TW (1967) The estuarine mycoflora. In: Lauff GH (ed) Estuaries, vol. 83. American Association for the Advancement of Science Publication, Washington, DC, USA, pp 303–305Google Scholar
  9. 9.
    Shearer CA (1972) Fungi of the chesapeake bay and its tributaries. III. The distribution of wood-inhabiting Ascomycetes and Fungi Imperfecti of the Patuxent River. Am J Bot 59(9):961–969CrossRefGoogle Scholar
  10. 10.
    Barghoorn E, Linder D (1944) Marine fungi: their taxonomy and biology. Farlowia 1(3):395–467Google Scholar
  11. 11.
    Kohlmeyer J, Kohlmeyer E (1979) Marine mycology: the higher fungi. Academic Press, New York, USAGoogle Scholar
  12. 12.
    Siepmann R, Johnson T (1960) Isolation and culture of fungi from wood submerged in saline and fresh waters. J Elisha Mitchell Sci Soc 76(1):150–154Google Scholar
  13. 13.
    Henningsson M (1974) Aquatic lignicolous fungi in the Baltic and along the west coast of Sweden. Svensk Bot Tidskr 68:401–425Google Scholar
  14. 14.
    Rämä T, Nordén J, Davey ML, Mathiassen GH, Spatafora JW, Kauserud H (2014) Fungi ahoy! Diversity on marine wooden substrata in the high North. Fungal Ecol 8:46–58. doi: 10.1016/j.funeco.2013.12.002 CrossRefGoogle Scholar
  15. 15.
    Jones EBG, Suetrong S, Sakayaroj J, Bahkali AH, Abdel-Wahab MA, Boekhout T, Pang K-L (2015) Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 73(1):1–72. doi: 10.1007/s13225-015-0339-4 CrossRefGoogle Scholar
  16. 16.
    Jones EBG, Pang K-L (2012) Introduction marine fungi. In: Jones EBG, Pang K-L (eds) Marine fungi and fungal-like organisms. Walter de Gruyter, Berlin, Germany, pp 1–13. doi: 10.1515/9783110264067.1 CrossRefGoogle Scholar
  17. 17.
    Jones EBG (2000) Marine fungi: some factors influencing biodiversity. Fungal Divers 4:53–73Google Scholar
  18. 18.
    Pang K-L, Chow R, Chan C, Vrijmoed L (2011) Diversity and physiology of marine lignicolous fungi in Arctic waters: a preliminary account. Polar Res 30:5859–5863. doi: 10.3402/polar.v30i0.5859 CrossRefGoogle Scholar
  19. 19.
    Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R, Kõljalg U, Pennanen T, Rosendahl S, Stenlid J, Kauserud H (2013) Fungal community analysis by high-throughput sequencing of amplified markers—a user's guide. New Phytol 199(1):288–299. doi: 10.1111/nph.12243 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ovaskainen O, Schigel D, Ali-Kovero H, Auvinen P, Paulin L, Nordén B, Nordén J (2013) Combining high-throughput sequencing with fruit body surveys reveals contrasting life-history strategies in fungi. ISME J 7(9):1696–1709. doi: 10.1038/ismej.2013.61 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Kubartová A, Ottosson E, Dahlberg A, Stenlid J (2012) Patterns of fungal communities among and within decaying logs, revealed by 454 sequencing. Mol Ecol 21(18):4514–4532. doi: 10.1111/j.1365-294X.2012.05723.x CrossRefPubMedGoogle Scholar
  22. 22.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118. doi: 10.1111/j.1365-294X.1993.tb00005.x CrossRefPubMedGoogle Scholar
  23. 23.
    White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322. doi: 10.1016/B978-0-12-372180-8.50042-1 Google Scholar
  24. 24.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. doi: 10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7(9):668–669. doi: 10.1038/nmeth0910-668b CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460–2461. doi: 10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  27. 27.
    Carlsen T, Aas AB, Lindner D, Vrålstad T, Schumacher T, Kauserud H (2012) Don’t make a mista(g)ke: is tag switching an overlooked source of error in amplicon pyrosequencing studies? Fungal Ecol 5(6):747–749. doi: 10.1016/j.funeco.2012.06.003 CrossRefGoogle Scholar
  28. 28.
    Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20(4):217–263. doi: 10.1007/s00572-009-0274-x CrossRefPubMedGoogle Scholar
  29. 29.
    Quince C, Lanzen A, Davenport R, Turnbaugh P (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38. doi: 10.1186/1471-2105-12-38
  30. 30.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. doi: 10.1128/aem.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    WoRMS Editorial Board (2012) World register of marine species. www.marinespecies.org. Accessed 1 October 2012
  32. 32.
    Whittaker RH (1960) Vegetation of the Siskiyou mountains, Oregon and California. Ecol Monogr 30(3):279–338. doi: 10.2307/1943563 CrossRefGoogle Scholar
  33. 33.
    Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, Longino JT (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol 5(1):3–21. doi: 10.1093/jpe/rtr044 CrossRefGoogle Scholar
  34. 34.
    Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9.1.0. www.purl.oclc.org/estimates. Accessed 10 December 2013
  35. 35.
    McCullagh P, Nelder JA (1989) Generalized linear models, vol 37. Chapmann & Hall, London, EnglandCrossRefGoogle Scholar
  36. 36.
    Crawley M (2013) The R book, 2nd edn. John Wiley & Sons, Sussex, UKGoogle Scholar
  37. 37.
    Legendre P, Legendre L (2012) Numerical ecology. Developments in environmental modelling, vol 24, 3rd edn. doi: 10.1016/B978-0-444-53868-0.50014-9
  38. 38.
    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2013) Vegan: Community Ecology Package. Version 2.0-10 edn.,Google Scholar
  39. 39.
    R Core Development Team (2014) R: a language and environment for statistical computing. Version 3.1.2 edn. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  40. 40.
    Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W.H. Freeman, New York, USAGoogle Scholar
  41. 41.
    Runnel K, Tamm H, Lõhmus A (2015) Surveying wood-inhabiting fungi: most molecularly detected polypore species form fruit-bodies within short distances. Fungal Ecol 18:93–99. doi: 10.1016/j.funeco.2015.08.008 CrossRefGoogle Scholar
  42. 42.
    Jones EBG (2011) Fifty years of marine mycology. Fungal Divers 50(1):73–112. doi: 10.1007/s13225-011-0119-8 CrossRefGoogle Scholar
  43. 43.
    Bellemain E, Carlsen T, Brochmann C, Coissac E, Taberlet P, Kauserud H (2010) ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases. BMC Microbiol 10(1):189CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Suetrong S, Jones EBG (2006) Marine discomycetes: a review. Ind J Mar Sci 35(4):291–296Google Scholar
  45. 45.
    Jones EBG (1994) Fungal adhesion. Mycol Res 98(9):961–981. doi: 10.1016/S0953-7562(09)80421-8 CrossRefGoogle Scholar
  46. 46.
    Nakagiri A, Ito T (1991) Basidiocarp development of the cyphelloid gasteroid aquatic basidiomycetes Halocyphina villosa and Limnoperdon incarnatum. Can J Botany 69(10):2320–2327. doi: 10.1139/b91-292 CrossRefGoogle Scholar
  47. 47.
    Hibbett DS, Binder M (2001) Evolution of marine mushrooms. Biol Bull 201(3):319–322. doi: 10.2307/1543610 CrossRefPubMedGoogle Scholar
  48. 48.
    Mouzouras R, Jones EBG, Venkatasamy R, Moss ST (1987) Decay of wood by microorganisms in marine environments. Record of the 1986 Annual Convention of the British Wood Preserving Association. Cambridge, UKGoogle Scholar
  49. 49.
    Jones EBG, Choeyklin R (2008) Ecology of marine and freshwater basidiomycetes. In: Boddy L, Frankland JC, van West P (eds) Ecology of saprotrophic basidiomycetes. Elsevier, Amsterdam, Netherlands, pp 301–324. doi: 10.1016/S0275-0287(08)80018-5 CrossRefGoogle Scholar
  50. 50.
    Duncan CG (1960) Wood-attacking capacities and physiology of soft-rot fungi. Report United States Forest Products Laboratory 2173Google Scholar
  51. 51.
    Petersen KRL, Koch J (1997) Substrate preference and vertical zonation of lignicolous marine fungi on mooring posts of Oak (Quercus sp.) and larch (Larix sp.) in Svanemøllen Harbour, Denmark. Bot Mar 40(1-6):451–464. doi: 10.1515/botm.1997.40.1-6.451 CrossRefGoogle Scholar
  52. 52.
    Maria G, Sridhar K (2003) Diversity of filamentous fungi on woody litter of five mangrove plant species from the southwest coast of India. Fungal Divers 14:109–126Google Scholar
  53. 53.
    Nordén J, Penttilä R, Siitonen J, Tomppo E, Ovaskainen O (2013) Specialist species of wood-inhabiting fungi struggle while generalists thrive in fragmented boreal forests. J Ecol 101(3):701–712. doi: 10.1111/1365-2745.12085 CrossRefGoogle Scholar
  54. 54.
    Yamashita S, Masuya H, Abe S, Masaki T, Okabe K (2015) Relationship between the decomposition process of coarse woody debris and fungal community structure as detected by high-throughput sequencing in a deciduous broad-leaved forest in Japan. PLoS One 10(6), e0131510. doi: 10.1371/journal.pone.0131510 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Hyde K (1989) Ecology of tropical marine fungi. Hydrobiologia 178(3):199–208. doi: 10.1007/BF00006027 CrossRefGoogle Scholar
  56. 56.
    Byrne P, Jones GEB (1975) Effect of salinity on spore germination of terrestrial and marine fungi. Trans Br Mycol Soc 64(3):497–503. doi: 10.1016/S0007-1536(75)80149-5 CrossRefGoogle Scholar
  57. 57.
    Hyde KD, Farrant CA, Jones EBG (1987) Isolation and culture of marine fungi. Bot Mar 30(4):291–303CrossRefGoogle Scholar
  58. 58.
    Nakagiri A (2012) Culture collections and maintenance of marine fungi. In: Jones EBG, Pang K-L (eds) Marine fungi and fungal-like organisms. Walter de Gruyter, Berlin, pp 501–507. doi: 10.1515/9783110264067.501 Google Scholar
  59. 59.
    Hughes GC (1974) Geographical distribution of the higher marine fungi. Veroeff Inst Meeresforsch Bremerhav Suppl 5:419–441Google Scholar
  60. 60.
    Booth T, Kenkel N (1986) Ecological studies of lignicolous marine fungi: a distribution model based on ordination and classification. In: Moss ST (ed) The biology of marine fungi. Cambridge University Press, Cambridge, England, pp 297–310Google Scholar
  61. 61.
    Panebianco C (1994) Temperature requirements of selected marine fungi. Bot Mar 37(2):157–162. doi: 10.1515/botm.1994.37.2.157 CrossRefGoogle Scholar
  62. 62.
    Wassmann P, Svendsen H, Keck A, Reigstad M (1996) Selected aspects of the physical oceanography and particle fluxes in fjords of northern Norway. J Mar Syst 8(1):53–71. doi: 10.1016/0924-7963(95)00037-2 CrossRefGoogle Scholar
  63. 63.
    Elliott JSB (1930) The soil fungi of the Dovey salt marshes. Ann Appl Biol 17(2):284–305. doi: 10.1111/j.1744-7348.1930.tb07215.x CrossRefGoogle Scholar
  64. 64.
    Alexander E, Stock A, Breiner H-W, Behnke A, Bunge J, Yakimov MM, Stoeck T (2009) Microbial eukaryotes in the hypersaline anoxic L’Atalante deep-sea basin. Environ Microbiol 11(2):360–381. doi: 10.1111/j.1462-2920.2008.01777.x CrossRefPubMedGoogle Scholar
  65. 65.
    Edgcomb VP, Beaudoin D, Gast R, Biddle JF, Teske A (2011) Marine subsurface eukaryotes: the fungal majority. Environ Microbiol 13(1):172–183. doi: 10.1111/j.1462-2920.2010.02318.x CrossRefPubMedGoogle Scholar
  66. 66.
    Orsi W, Biddle JF, Edgcomb V (2013) Deep sequencing of subseafloor eukaryotic rRNA reveals active fungi across marine subsurface provinces. PLoS One 8(2), e56335. doi: 10.1371/journal.pone.0056335 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Ramírez-Camejo LA, Zuluaga-Montero A, Lázaro-Escudero M, Hernández-Kendall V, Bayman P (2012) Phylogeography of the cosmopolitan fungus Aspergillus flavus: is everything everywhere? Fungal Biol 116(3):452–463. doi: 10.1016/j.funbio.2012.01.006 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Teppo Rämä
    • 1
    • 2
  • Marie L. Davey
    • 3
    • 4
    • 5
  • Jenni Nordén
    • 3
    • 6
    • 7
  • Rune Halvorsen
    • 6
  • Rakel Blaalid
    • 3
    • 8
  • Geir H. Mathiassen
    • 1
  • Inger G. Alsos
    • 1
  • Håvard Kauserud
    • 3
  1. 1.Tromsø University MuseumUiT The Arctic University of NorwayTromsøNorway
  2. 2.MarbioUiT The Arctic University of NorwayTromsøNorway
  3. 3.Section for Genetics and Evolutionary Biology, Department of BiosciencesUniversity of OsloOsloNorway
  4. 4.Department of Ecology and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway
  5. 5.University Centre in Svalbard (UNIS)SvalbardNorway
  6. 6.Natural History MuseumUniversity of OsloOsloNorway
  7. 7.Norwegian Institute for Nature ResearchOsloNorway
  8. 8.Haukeland University HospitalBergenNorway

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