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Distinct sensitivity of fungal freshwater guilds to water quality

Mycological Progress volume 16, pages 155–169 (2017)Cite this article

Abstract

Multiple anthropogenic stressors have been shown to impact animal and plant communities in freshwater ecosystems, but the responses of aquatic fungi remain largely unknown. Stressor effects on fungal communities may, however, result in changes of decomposition of plant litter and, thus, impact nutrient cycling, a key process for ecosystem functioning. We tested the impact of increased chloride and sediment levels, as well as reduced water flow velocity, on eukaryotic freshwater communities, with an emphasis on fungi, in a mesocosm experiment. Each of the three stressors was applied individually and in all combinations in a full-factorial design. Litterbags with non-sterilised tree leaves and sterile ceramic tiles were added to the mesocosms, to analyse the responses of communities in decaying plant material and in biofilms. Fungi preferably occurring in biofilms were supposed to represent indigenous aquatic fungi, while litterbag communities should be predominantly composed of fungi known from terrestrial litter. Community composition was assessed by high-throughput sequencing of amplified barcoding regions. Similarity matrices of operational taxonomic unit (OTU) tables calculated by UCLUST and CD-HIT-OTU-Illumina were significantly correlated. Preferred occurrence in biofilm and litter communities, respectively, was used for the grouping of OTUs into three ecological guilds. Stressor sensitivity varied among the guilds. While non-fungal, in particular autotrophic, OTUs responded to several treatments, two of the fungal guilds, i.e. those exclusively colonising litter and those preferably occurring on the ceramic tiles, showed no response to any applied treatment. Only fungi preferably, but not exclusively, colonising litter significantly responded to chloride addition. Their distribution patterns again correlated significantly with those of non-fungal OTUs, indicating possible interdependencies between both groups. The results indicate that eukaryotic freshwater communities are composed of different guilds, with distinctive sensitivity and tolerance to anthropogenic stressors.

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References

  • Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565

    Article  CAS  PubMed  Google Scholar 

  • Artigas J, Romaní AM, Sabater S (2008) Effect of nutrients on the sporulation and diversity of aquatic hyphomycetes on submerged substrata in a Mediterranean stream. Aquat Bot 88:32–38

    Article  CAS  Google Scholar 

  • Baldrian P, Větrovský T, Cajthaml T, DobiáŠová P, Petránková M, Šnajdr J, Eichlerová I (2013) Estimation of fungal biomass in forest litter and soil. Fungal Ecol 6:1–11

    Article  Google Scholar 

  • Bärlocher F (2016) Aquatic fungal ecology. Fungal Ecol 19:1–4

    Article  Google Scholar 

  • Bässler C, Müller J, Cadotte MW, Heibl C, Bradtka JH, Thorn S, Halbwachs H (2016) Functional response of lignicolous fungal guilds to bark beetle deforestation. Ecol Indic 65:149–150

    Article  Google Scholar 

  • Bauer R, Begerow D, Oberwinkler F, Marvanová L (2003) Classicula: the teleomorph of Naiadella fluitans. Mycologia 95:756–764

    Article  PubMed  Google Scholar 

  • Belliveau MJR, Bärlocher F (2005) Molecular evidence confirms multiple origins of aquatic hyphomycetes. Mycol Res 109:1407–1417

    Article  CAS  PubMed  Google Scholar 

  • Benner R, Moran MA, Hodson RE (1986) Biogeochemical cycling of lignocellulosic carbon in marine and freshwater ecosystems: Relative contributions of procaryotes and eucaryotes. Limnol Oceanogr 31:89–100

    Article  Google Scholar 

  • Blackwell M (2011) The fungi: 1, 2, 3… 5.1 million species? Am J Bot 98:426–438

    Article  PubMed  Google Scholar 

  • Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    Article  CAS  PubMed  Google Scholar 

  • Bouraoui F, Grizzetti B, Adelsköld G, Behrendt H, De Miguel I, Silgram M, Gómez S, Granlund K, Hoffmann L, Kronvang B, Kværnø S, Lázár A, Mimikou M, Passarella G, Panagos P, Reisser H, Schwarzl B, Siderius C, Sileika AS, Smit AA, Sugrue R, Vanliedekerke M, Zaloudik J (2009) Basin characteristics and nutrient losses: the EUROHARP catchment network perspective. J Environ Monit 11:515–525

    Article  CAS  PubMed  Google Scholar 

  • Brown SP, Veach AM, Rigdon-Huss AR, Grond K, Lickteig SK, Lothamer K, Oliver AK, Jumpponen A (2014) Scraping the bottom of the barrel: are rare high throughput sequences artifacts? Fungal Ecol 13:221–225

    Article  Google Scholar 

  • Bucher VVC, Hyde KD, Pointing SB, Reddy CA (2004) Production of wood decay enzymes, mass loss and lignin solubilization in wood by marine ascomycetes and their anamorphs. Fungal Divers 15:1–14

    Google Scholar 

  • Byrne PJ, Jones EBG (1975) Effect of salinity on the reproduction of terrestrial and marine fungi. Trans Br Mycol Res 65:185–200

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carney LT, Lane TW (2014) Parasites in algae mass culture. Front Microbiol 5:1–8

    Article  Google Scholar 

  • Chan SY, Goh TK, Hyde KD (2000) Ingoldian fungi in Lam Tsuen River and Tai Po Kau Forest Stream, Hong Kong. Fungal Divers 5:109–118

    Google Scholar 

  • Chauvet E, Cornut J, Sridhar KR, Selosse MA, Bärlocher F (2016) Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecol 19:112–127

    Article  Google Scholar 

  • Clarke KR, Chapman MG, Somerfield PJ, Needham HR (2006a) Dispersion-based weighting of species counts in assemblage analyses. Mar Ecol Prog Ser 320:11–27

    Article  Google Scholar 

  • Clarke KR, Somerfield PJ, Chapman MG (2006b) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80

    Article  Google Scholar 

  • Colas F, Baudoin JM, Chauvet E, Clivot H, Danger M, Guérold F, Devin S (2016) Dam-associated multiple-stressor impacts on fungal biomass and richness reveal the initial signs of ecosystem functioning impairment. Ecol Indic 60:1077–1090

    Article  Google Scholar 

  • Crowther TW, Maynard DS, Crowther TR, Peccia J, Smith JR, Bradford MA (2014) Untangling the fungal niche: the trait-based approach. Front Microbiol 5:579

    Article  PubMed  PubMed Central  Google Scholar 

  • de Graaff MA, Classen AT, Castro HF, Schadt CW (2010) Labile soil carbon inputs mediate the soil microbial community composition and plant residue decomposition rates. New Phytol 188:1055–1064

    Article  PubMed  CAS  Google Scholar 

  • de Menezes AB, Prendergast-Miller MT, Richardson AE, Toscas P, Farrell M, Macdonald LM, Baker G, Wark T, Thrall PH (2014) Network analysis reveals that bacteria and fungi form modules that correlate independently with soil parameters. Environ Microbiol 17:2677–2689

    Article  PubMed  CAS  Google Scholar 

  • de Vries FT, Bloem J, Quirk H, Stevens CJ, Bol R, Bardgett RD (2012) Extensive management promotes plant and microbial nitrogen retention in temperate grassland. PLoS One 7:1–12

    Google Scholar 

  • Dong D, Yan A, Liu H, Zhang X, Xu Y (2006) Removal of humic substances from soil DNA using aluminium sulfate. J Microbiol Meth 66:217–222

    Article  CAS  Google Scholar 

  • Duarte S, Bärlocher F, Trabulo J, Cássio F, Pascoal C (2015) Stream-dwelling fungal decomposer communities along a gradient of eutrophication unraveled by 454 pyrosequencing. Fungal Divers 70:127–148

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Flyvbjerg H (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482

    Article  CAS  PubMed  Google Scholar 

  • Elbrecht V, Beermann AJ, Goessler G, Neumann J, Tollrian R, Wagner R, Wlecklik A, Piggott JJ, Matthaei CD, Leese F (2016) Multiple-stressor effects on stream invertebrates: a mesocosm experiment manipulating nutrients, fine sediment and flow velocity. Freshw Biol 61:362–375

    Article  Google Scholar 

  • Fernandes I, Seena S, Pascoal C, Cássio F (2014) Elevated temperature may intensify the positive effects of nutrients on microbial decomposition in streams. Freshw Biol 59:2390–2399

    Article  CAS  Google Scholar 

  • Ferreira V, Graça MAS (2016) Effects of whole-stream nitrogen enrichment and litter species mixing on litter decomposition and associated fungi. Limnologica 58:69–77

    Article  CAS  Google Scholar 

  • Ferreira V, Gulis V, Graça MAS (2006) Whole-stream nitrate addition affects litter decomposition and associated fungi but not invertebrates. Oecologia 149:718–729

    Article  PubMed  Google Scholar 

  • Gathe SD, Sridhar KR (2015) A new technique to monitor conidia of aquatic hyphomycetes in streams using latex-coated slides. Mycology 6:3–4

  • Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380

    Article  PubMed  Google Scholar 

  • Goh TK, Hyde KD (1996) Biodiversity of freshwater fungi. J Ind Microbiol Biotechnol 17:328–345

    Article  CAS  Google Scholar 

  • Gönczöl J, Révay Á (2003) Treehole fungal communities: aquatic, aero-aquatic and dematiaceous hyphomycetes. Fungal Divers 12:19–34

    Google Scholar 

  • Gönczöl J, Révay Á (2006) Species diversity of rainborne hyphomycete conidia from living trees. Fungal Divers 22:37–54

    Google Scholar 

  • Graça MAS, Ferreira V, Canhoto C, Encalada AC, Guerrero-Bolaño F, Wantzen KM, Boyero L (2015) A conceptual model of litter breakdown in low order streams. Int Rev Hydrobiol 100:1–12

    Article  CAS  Google Scholar 

  • Graça MAS, Hyde K, Chauvet E (2016) Aquatic hyphomycetes and litter decomposition in tropical–subtropical low order streams. Fungal Ecol 19:182–189

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Grossart HP, Wurzbacher C, James TY, Kagami M (2016) Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecol 19:28–38

    Article  Google Scholar 

  • Hammel KE (1997) Fungal degradation of lignin. In: Cadisch G, Giller KE (eds) Driven by nature: plant litter quality and decomposition. CAB International, Wallingford, UK, pp 33–46

    Google Scholar 

  • Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol Res 105:1422–1432

    Article  Google Scholar 

  • Hulsen T, de Vlieg J, Alkema W (2008) BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:1–6

    Article  CAS  Google Scholar 

  • Hyde KD, Fryar S, Tian Q, Bahkali AH, Xu J (2015) Lignicolous freshwater fungi along a north-south latitudinal gradient in the Asian/Australien region; can we predict the impact of global warming on biodiversity and function? Fungal Ecol 1–9

  • Hyde KD, Fryar S, Tian Q, Bahkali AH, Xu J (2016) Lignicolous freshwater fungi along a north–south latitudinal gradient in the Asian/Australian region; can we predict the impact of global warming on biodiversity and function? Fungal Ecol 19:190–200

    Article  Google Scholar 

  • Ingold CT (1942) Aquatic hyphomycetes of decaying alder leaves. Trans Br Mycol Soc 25:339–417

    Article  Google Scholar 

  • Ingold CT (1953) Dispersal in fungi. Oxford University Press, Amen House, London

    Google Scholar 

  • Jackson MC, Loewen CJ, Vinebrooke RD, Chimimba CT (2016) Net effects of multiple stressors in freshwater ecosystems: a meta-analysis. Glob Chang Biol 22:180–189

    Article  PubMed  Google Scholar 

  • Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearns SG, Bärlocher F (2008) Leaf surface roughness influences colonization success of aquatic hyphomycete conidia. Fungal Ecol 1:13–18

    Article  Google Scholar 

  • Kodsueb R, Lumyong S, McKenzie EHC, Bahkali AH, Hyde KD (2016) Relationships between terrestrial and freshwater lignicolous fungi. Fungal Ecol 19:155–168

    Article  Google Scholar 

  • Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vrålstad T, Ursing BM (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068

    Article  PubMed  CAS  Google Scholar 

  • Krauss GJ, Solé M, Krauss G, Schlosser D, Wesenberg D, Bärlocher F (2011) Fungi in freshwaters: ecology, physiology and biochemical potential. FEMS Microbiol Rev 35:620–651

    Article  CAS  PubMed  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleici acid techniques in bacterial systematics. John Wiley & Sons, New York, pp 115–147

  • Lange K, Liess A, Piggott JJ, Townsend CR, Matthaei CD (2011) Light, nutrients and grazing interact to determine stream diatom community composition and functional group structure. Freshw Biol 56:264–278

    Article  Google Scholar 

  • Lange A, Jost S, Heider D, Bock C, Budeus B, Schilling E, Strittmatter A, Boenigk J, Hoffmann D (2015) AmpliconDuo: a split-sample filtering protocol for high-throughput amplicon sequencing of microbial communities. PLoS One 10:1–22

    Google Scholar 

  • Lechat C, Fournier J (2015) Varicosporella, a new aquatic genus in the Nectriaceae from France. Ascomycete.org 7:1–8

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Li W, Fu L, Niu B, Wu S, Wooley J (2012) Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 13:656–668

    Article  PubMed  PubMed Central  Google Scholar 

  • McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:1–14

    Article  CAS  Google Scholar 

  • Medeiros AO, Pascoal C, Graça MAS (2009) Diversity and activity of aquatic fungi under low oxygen conditions. Freshw Biol 54:142–149

    Article  Google Scholar 

  • Menkis A, Marčiulynas A, Gedminas A, Lynikiené J, Povilaitiené A (2015) High-throughput sequencing reveals drastic changes in fungal communities in the phyllosphere of Norway spruce (Picea abies) following invasion of the spruce bud scale (Physokermes piceae). Microb Ecol 70:904–911

    Article  CAS  PubMed  Google Scholar 

  • Nielsen DL, Brock MA, Crosslé K, Harris K, Healey M, Jarosinski I (2003a) The effects of salinity on aquatic plant germination and zooplankton hatching from two wetland sediments. Freshw Biol 48:2214–2223

    Article  Google Scholar 

  • Nielsen DL, Brock MA, Rees GN, Baldwin DS (2003b) Effects of increasing salinity on freshwater ecosystems in Australia. Aust J Bot 51:655–665

    Article  Google Scholar 

  • Nikolcheva LG, Bärlocher F (2005) Seasonal and substrate preferences of fungi colonizing leaves in streams: traditional versus molecular evidence. Environ Microbiol 7:270–280

    Article  CAS  PubMed  Google Scholar 

  • Ochoa AIDA, Ferreira V, Graça MAS (2012) The performance of biological indicators in assessing the ecological state of streams with varying catchment urbanisation levels in Coimbra, Portugal. Limnetica 31:141–154

    Google Scholar 

  • Overy DP, Bayman P, Kerr RG, Bills GF (2014) An assessment of natural product discovery from marine (sensu strictu) and marine-derived fungi. Mycology 5:145–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Pascoal C, Cássio F, Marcotegui A, Sanz B, Gomes P (2005) Role of fungi, bacteria, and invertebrates in leaf litter breakdown in a polluted river. J North Am Benthol Soc 24:784–797

    Article  Google Scholar 

  • Peay KG, Kennedy PG, Talbot JM (2016) Dimensions of biodiversity in the Earth mycobiome. Nature 14:434–447

    CAS  Google Scholar 

  • Peršoh D (2015) Plant-associated fungal communities in the light of meta’omics. Fungal Divers 75:1–25

    Article  Google Scholar 

  • Peršoh D, Theuerl S, Buscot F, Rambold G (2008) Towards a universally adaptable method for quantitative extraction of high-purity nucleic acids from soil. J Mircobiol Meth 75:19–24

    Article  CAS  Google Scholar 

  • Piggott JJ, Salis RK, Lear G, Townsend CR, Matthaei CD (2015a) Climate warming and agricultural stressors interact to determine stream periphyton community composition. Glob Chang Biol 21:206–222

    Article  PubMed  Google Scholar 

  • Piggott JJ, Townsend CR, Matthaei CD (2015b) Climate warming and agricultural stressors interact to determine stream macroinvertebrate community dynamics. Glob Chang Biol 21:1887–1906

    Article  PubMed  Google Scholar 

  • Piggott JJ, Townsend CR, Matthaei CD (2015c) Reconceptualizing synergism and antagonism among multiple stressors. Ecol Evol 5:1535–1547

    Article  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Home page at: http://www.R-project.org/

  • Raja HA, Oberlies NH, Figueroa M, Tanaka K, Hirayama K, Hashimoto A, Miller AN, Zelski SE, Shearer CA (2013) Freshwater ascomycetes: Minutisphaera (Dothideomycetes) revisited, including one new species from Japan. Mycologia 105:959–976

    Article  PubMed  Google Scholar 

  • Raviraja NS, Sridhar KR, Bärlocher F (1996) Endophytic aquatic hyphomycetes of roots of plantation crops and ferns from India. Sydowia 48:152–160

    Google Scholar 

  • Sati SC, Belwal M (2005) Aquatic hyphomycetes as endophytes of riparian plant roots. Mycologia 97:45–49

    Article  CAS  PubMed  Google Scholar 

  • Sati SC, Belwal M, Pargaein N (2008) Diversity of water borne conidial fungi as root endophytes in temperate forest plants of western Himalaya. Nat Sci 6:59–65

    Google Scholar 

  • Schmit JP, Mueller GM (2007) An estimate of the lower limit of global fungal diversity. Biodivers Conserv 16:99–111

    Article  Google Scholar 

  • Schmidt PA, Bálint M, Greshake B, Bandow C, Römbke J, Schmitt I (2013) Illumina metabarcoding of a soil fungal community. Soil Biol Biochem 65:128–132

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  Google Scholar 

  • Seena S, Monroy S (2016) Preliminary insights into the evolutionary relationships of aquatic hyphomycetes and endophytic fungi. Fungal Ecol 19:128–134

    Article  Google Scholar 

  • Shearer CA, Webster J (1991) Aquatic hyphomycete communities in the river Teign. IV. Twig colonization. Mycol Res 95:413–420

    Article  Google Scholar 

  • Shearer CA, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanová L, Padgett D, Porter D, Raja HA, Schmit JP, Thorton HA, Voglymayr H (2007) Fungal biodiversity in aquatic habitats. Biodivers Conserv 16:49–67

    Article  Google Scholar 

  • Shearer CA, Zelski SE, Raja HA, Schmit JP, Miller AN, Janovec JP (2015) Distributional patterns of freshwater ascomycetes communities along an Andes to Amazon elevational gradient in Peru. Biodivers Conserv 24:1877–1897

    Article  Google Scholar 

  • Sinclair L, Osman OA, Bertilsson S, Eiler A (2015) Microbial community composition and diversity via 16S rRNA gene amplicons: Evaluating the illumina platform. PLoS One 10:1–18

    Google Scholar 

  • Smith DP, Peay KG (2014) Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS One 9:1–12

    Google Scholar 

  • Solé M, Fetzer I, Wennrich R, Sridhar KR, Harms H, Krauss G (2008) Aquatic hyphomycete communities as potential bioindicators for assessing anthropogenic stress. Sci Total Environ 389:557–565

    Article  PubMed  CAS  Google Scholar 

  • Stefani FOP, Bell TH, Marchand C, de la Providencia IE, El Yassimi A, St-Arnaud M, Hijri M (2015) Culture-dependent and -independent methods capture different microbial community fractions in hydrocarbon-contaminated soils. PLoS One 10:1–16

    Google Scholar 

  • Stielow JB, Lévesque CA, Seifert KA, Meyer W, Iriny L, Smits D et al (2015) One fungus, which genes? Development and assessment of universal primers for potential secondary fungal DNA barcodes. Persoonia 35:242–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liao HL, Smith ME, Peay KG (2014) Endemism and functional convergence across the North American soil mycobiome. Proc Natl Acad Sci U S A 111:6341–6346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tank JL, Dodds WK (2003) Nutrient limitation of epilithic and epixylic biofilms in ten North American streams. Freshw Biol 48:1031–1049

    Article  CAS  Google Scholar 

  • Tedersoo L, Bahram M, Põlme S, Kõljalg U, Yorou NS, Wijesundera R et al (2014) Global diversity and geography of soil fungi. Science 346:1078–1088

    Article  CAS  Google Scholar 

  • Thomsen PF, Willerslev E (2015) Environmental DNA—an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18

    Article  Google Scholar 

  • Toju H, Sato H, Tanabe AS (2014) Diversity and spatial structure of belowground plant–fungal symbiosis in a mixed subtropical forest of ectomycorrhizal and arbuscular mycorrhizal plants. PLoS One 9:24–26

    Article  CAS  Google Scholar 

  • Urbina H, Scofield DG, Cafaro M, Rosling A (2016) DNA-metabarcoding uncovers the diversity of soil-inhabiting fungi in the tropical island of Puerto Rico. Mycoscience 57:217–227

    Article  CAS  Google Scholar 

  • Vijaykrishna D, Jeewon R, Hyde KD (2006) Molecular taxonomy, origins and evolution of freshwater ascomycetes. Fungal Divers 23:351–390

    Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (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, vol 38. Academic Press, New York, NY, pp 315–322

    Google Scholar 

  • Wu S, Zhu Z, Fu L, Niu B, Li W (2011) WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12:1–9

    Article  CAS  Google Scholar 

  • Yuen TK, Hyde KD, Hodgkiss IJ (1998) Physiological growth parameters and enzyme production in tropical freshwater fungi. Mater Org 32:2–16

    Google Scholar 

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Acknowledgements

We would like to thank Janis Neumann, Andre Wlecklik and Christoph Thiel (UDE, AG Aquatic ecosystem research) for assisting with the mesocosm experiment and collecting the samples. We would like to thank Tanja Rollnik (RUB, AG Geobotany) for the DNA extraction and library preparation. We would also like to thank Manfred Jensen (UDE, AG Aquatic ecosystem research) and Christian Schulz (RUB, Department of Botany) for the helpful discussions regarding the appropriate statistical analysis. Hai Nguyen is thanked for critically reading the manuscript and linguistic improvement. Finally, we would like to thank Stiftung Mercator (Pr-2013-0036) and the Kurt Eberhard Bode Foundation (FL) for the financial support. FL and VE would like to thank Jeremy Piggott (University of Kyoto), Christoph Matthaei (University of Otago) and Ralph Tollrian (University of Bochum) for the helpful advice during the planning of the ExStream experiment.

Author contributions

OR did the molecular work and data analyses. JN supported analysis of the biofilm samples. DP and MM performed the data analyses. AB and DP designed the HTS approach. DB and DP conceived the manuscript outline. VE and FL designed and coordinated the ExStream mesocosm experiment. JB and DB designed the microbial part of the experiment. OR wrote the manuscript, with the guidance and support of DB and DP. All authors discussed and commented on the final version of the manuscript.

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  1. AG Geobotany, Faculty of Biology and Biotechnology, Ruhr-Universität Bochum, Universitätsstr. 150, 44801, Bochum, Germany

    Oliver Röhl, Derek Peršoh, Moritz Mittelbach & Dominik Begerow

  2. AG Aquatic Ecosystem Research, Faculty of Biology, Universität Duisburg-Essen, Universitätsstr. 5, 45141, Essen, Germany

    Vasco Elbrecht & Florian Leese

  3. Genetics, Faculty of Biology, Ludwig-Maximilians-University Munich, Großhaderner Straße 2–4, 82152, Planegg-Martinsried, Germany

    Andreas Brachmann

  4. Department of Biodiversity, Faculty of Biology, Universität Duisburg-Essen, Universitätsstr. 5, 45141, Essen, Germany

    Julia Nuy & Jens Boenigk

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  1. Oliver Röhl
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Correspondence to Oliver Röhl.

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Röhl, O., Peršoh, D., Mittelbach, M. et al. Distinct sensitivity of fungal freshwater guilds to water quality. Mycol Progress 16, 155–169 (2017). https://doi.org/10.1007/s11557-016-1261-1

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  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-016-1261-1

Keywords

  • Fungal guilds
  • Freshwater fungi
  • Abiotic stressors
  • OTU diversity