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Nutrient Enrichment Alters Salt Marsh Fungal Communities and Promotes Putative Fungal Denitrifiers

Abstract

Enrichment of ecosystems with excess nutrients is occurring at an alarming rate and has fundamentally altered ecosystems worldwide. Salt marshes, which lie at the land-sea interface, are highly effective at removing anthropogenic nutrients through the action of macrophytes and through microbial processes in coastal sediments. The response of salt marsh bacteria to excess nitrogen has been documented; however, the role of fungi and their response to excess nitrogen in salt marsh sediments is not fully understood. Here, we document the response of salt marsh fungal communities to long-term excess nitrate in four distinct marsh habitats within a northern temperate marsh complex. We show that salt marsh fungal communities varied as a function of salt marsh habitat, with both fungal abundance and diversity increasing with carbon quantity. Nutrient enrichment altered fungal communities in all habitats through an increase in fungal abundance and the proliferation of putative fungal denitrifiers. Nutrient enrichment also altered marsh carbon quality in low marsh surface sediments where fungal response to nutrient enrichment was most dramatic, suggesting nutrient enrichment can alter organic matter quality in coastal sediments. Our results indicate that fungi, in addition to bacteria, likely play an important role in anaerobic decomposition of salt marsh sediment organic matter.

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References

  1. Galloway JN (1998) The global nitrogen cycle: changes and consequences. Nitrogen, the Confer-N-s. Elsevier, Amsterdam, pp 15–24

    Chapter  Google Scholar 

  2. Nixon SW, Oviatt CA, Frithsen J, Sullivan B (1986) Nutrients and the productivity of estuarine and coastal marine ecosystems. J Limnol Soc S Afr 12:43–71

    CAS  Google Scholar 

  3. Paerl HW (1997) Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as “new” nitrogen and other nutrient sources. Limnol Oceanogr 42:1154–1165

    Article  CAS  Google Scholar 

  4. Valiela I, Teal JM, Sass W (1973) Nutrient retention in salt marsh plots experimentally fertilized with sewage sludge. Estuarine Coastal Mar Sci 1:261–269

    Article  Google Scholar 

  5. Elahi R, O’Connor MI, Byrnes JEK, Dunic J, Eriksson BK, Hensel MJS, Kearns PJ (2015) Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr Biol 25:1938–1943

    Article  PubMed  CAS  Google Scholar 

  6. Koop-Jakobsen K, Giblin AE (2010) The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnol Oceanogr 55:789–802

    Article  CAS  Google Scholar 

  7. Rabalais NN, Turner RE, Wiseman Jr WJ (2002) Gulf of Mexico hypoxia, aka “The dead zone”. Annu Rev Ecol Syst 33:235–263

    Article  Google Scholar 

  8. Brin LD, Valiela I, Goehringer D, Howes B (2010) Nitrogen interception and export by experimental salt marsh plots exposed to chronic nutrient addition. Mar Ecol Prog Ser 400:3–17

    Article  CAS  Google Scholar 

  9. Carpenter EJ, Capone DG (2016) Nitrogen in the marine environment. Elsevier

  10. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616

    PubMed  PubMed Central  CAS  Google Scholar 

  11. Howes BL, Weiskel PK, Goehringer DD, Teal JM (1996) Interception of freshwater and nitrogen transport from uplands to coastal waters: the role of saltmarshes. Estuarine shores: evolution, environments and human alterations. Wiley, pp 287–310

  12. Valiela I, Teal JM (1979) The nitrogen budget of a salt marsh ecosystem. Nature 280:652–656

    Article  CAS  Google Scholar 

  13. McLeod E, Chmura GL, Bouillon S et al (2011) A blueprint for blue carbon: toward an improved understanding of the role of vegetated coastal habitats in sequestering CO2. Front. Ecol. Environ. 9:552–560

    Article  Google Scholar 

  14. Newell SY (1993) Decomposition of shoots of a salt-marsh grass. In: Jones JG (ed) Advances in microbial ecology. Springer US, Boston, MA, pp 301–326

    Chapter  Google Scholar 

  15. Benner R, Newell SY, Maccubbin AE, Hodson RE (1984) Relative contributions of bacteria and fungi to rates of degradation of lignocellulosic detritus in salt-marsh sediments. Appl. Environ. Microbiol. 48:36–40

    PubMed  PubMed Central  CAS  Google Scholar 

  16. Bergbauer M, Newell SY (1992) Contribution to lignocellulose degradation and DOC formation from a salt marsh macrophyte by the ascomycete Phaeosphaeria spartinicola. FEMS Microbiol Ecol 9:341–347

    Article  Google Scholar 

  17. Buchan A, Newell SY, Butler M, Biers EJ, Hollibaugh JT, Moran MA (2003) Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl Environ Microbiol. 69:6676–6687

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Kirwan ML, Mudd SM (2012) Response of salt-marsh carbon accumulation to climate change. Nature 489:550–553

    Article  PubMed  CAS  Google Scholar 

  19. Deegan LA, Johnson DS, Warren RS et al (2012) Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–392

    Article  PubMed  CAS  Google Scholar 

  20. Valiela I, Teal JM, Allen SD, van Etten R, Goehringer D, Volkmann S (1985) Decomposition in salt marsh ecosystems: the phases and major factors affecting disappearance of above-ground organic matter. J Exp Mar Bio Ecol 89:29–54

    Article  CAS  Google Scholar 

  21. Buchan A, Newell SY, Moreta JI, Moran MA (2002) Molecular characterization of bacterial and fungal decomposer communities in a southeastern US saltmarsh. Microb Ecol 43:329–340

    Article  PubMed  CAS  Google Scholar 

  22. Newell SY, Arsuffi TL, Palm LA (1996) Misting and nitrogen fertilization of shoots of a saltmarsh grass: effects upon fungal decay of leaf blades. Oecologia 108:495–502

    Article  PubMed  Google Scholar 

  23. Newell SY, Porter D, Lingle WL (1996) Lignocellulolysis by ascomycetes (fungi) of a saltmarsh grass (smooth cordgrass). Microsc Res Tech. 33:32–46

    Article  PubMed  CAS  Google Scholar 

  24. Newell SY (2001) Multiyear patterns of fungal biomass dynamics and productivity within naturally decaying smooth cordgrass shoots. Limnol Oceanogr 46:573–583

    Article  Google Scholar 

  25. Newell SY, Blum LK, Crawford RE, Dai T, Dionne M (2000) Autumnal biomass and potential productivity of salt marsh fungi from 29 to 43 north latitude along the United States Atlantic Coast. Appl Environ Microbiol 66:180–185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Torzilli AP, Sikaroodi M, Chalkley D, Gillevet PM (2006) A comparison of fungal communities from four salt marsh plants using automated ribosomal intergenic spacer analysis (ARISA). Mycologia 98:690–698

    Article  PubMed  CAS  Google Scholar 

  27. Ainsworth GC (2008) Ainsworth & Bisby’s dictionary of the fungi. CABI

  28. Richards TA, MDM J, Leonard G, Bass D (2012) Marine fungi: their ecology and molecular diversity. Annu Rev Mar Sci. 4:495–522

    Article  Google Scholar 

  29. Kis-Papo T (2005) Marine fungal communities. Mycol Ser. 23:61

    Article  Google Scholar 

  30. Dini-Andreote F, Pylro VS, Baldrian P et al (2016) Ecological succession reveals potential signatures of marine–terrestrial transition in salt marsh fungal communities. ISME J 10:1–14

    Article  CAS  Google Scholar 

  31. Taylor JD, Cunliffe M (2016) Multi-year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J 10:1–11

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  33. Bertness MD (1991) Zonation of Spartina patens and Spartina alterniflora in New England salt marsh. Ecology 72:138–148

    Article  Google Scholar 

  34. Levine JM, Brewer JS, Bertness MD (1998) Nutrients, competition and plant zonation in a New England salt marsh. J Ecol 86:285–292

    Article  Google Scholar 

  35. Crain CM, Silliman BR, Bertness SL, Bertness MD (2004) Physical and biotic drivers of plant distribution across estuarine salinity gradients. Ecology 85:2539–2549

    Article  Google Scholar 

  36. Johnson DS, Warren RS, Deegan LA, Mozdzer TJ (2016) Saltmarsh plant responses to eutrophication. Ecol Appl 26:2647–2659

    PubMed  Google Scholar 

  37. Deegan LA, Bowen JL, Drake D et al (2007) Susceptibility of salt marshes to nutrient enrichment and predator removal. Ecol Appl 17:s42–s63

    Article  Google Scholar 

  38. Bowen JL, Ward BB, Morrison HG, Hobbie JE, Valiela I, Deegan LA, Sogin ML (2011) Microbial community composition in sediments resists perturbation by nutrient enrichment. ISME J 5:1540–1548

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kearns PJ, Angell JH, Howard EM et al (2016) Nutrient enrichment induces dormancy and decreases diversity of active bacteria in salt marsh sediments. Nat. Commun. 7:1–9

    Article  CAS  Google Scholar 

  40. Bowen JL, Crump BC, Deegan LA, Hobbie JE (2009) Salt marsh sediment bacteria: their distribution and response to external nutrient inputs. ISME J 3:924–934

    Article  PubMed  CAS  Google Scholar 

  41. Walters W, Hyde ER, Berg-Lyons D et al (2016) Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1. https://doi.org/10.1128/mSystems.00009-15

  42. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Team, R Core (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing

  44. Oksanen J, Kindt R, Legendre P et al (2007) The vegan package. Community ecology package, vol 10, pp 631–637

    Google Scholar 

  45. Margenot AJ, Calderón FJ, Bowles TM, Parikh SJ, Jackson LE (2015) Soil organic matter functional group composition in relation to organic carbon, nitrogen, and phosphorus fractions in organically managed tomato fields. Soil Sci Soc Am J 79:772–782

    Article  CAS  Google Scholar 

  46. Margenot AJ, Calderon FJ, Parikh SJ (2016) Limitations and potential of spectral subtractions in Fourier-transform infrared spectroscopy of soil samples. Soil Sci Soc Am J 80:10–26

    Article  CAS  Google Scholar 

  47. Hsu J-H, Lo S-L (1999) Chemical and spectroscopic analysis of organic matter transformations during composting of pig manure. Environ. Pollut. 104:189–196

    Article  CAS  Google Scholar 

  48. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña 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  PubMed  PubMed Central  CAS  Google Scholar 

  49. Aronesty E (2011) ea-utils: command-line tools for processing biological sequencing data. Expression Analysis, Durham

    Google Scholar 

  50. Bokulich NA, Subramanian S, Faith JJ et al (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Bengtsson-Palme J, Ryberg M, Hartmann M et al (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919

    Google Scholar 

  53. Abarenkov K, Henrik Nilsson R, Larsson K-H, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Kõljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol. 186:281–285

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  55. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  56. Maeda K, Spor A, Edel-Hermann V, Heraud C, Breuil MC, Bizouard F, Toyoda S, Yoshida N, Steinberg C, Philippot L (2015) N2O production, a widespread trait in fungi. Sci. Rep. 5:9697

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Kearns PJ, Fischer S, Fernández-Beaskoetxea S et al (2017) Fight fungi with fungi: antifungal properties of the amphibian mycobiome. Front. Microbiol. 8:1–12

    Article  Google Scholar 

  58. Bardgett RD, Freeman C, Ostle NJ (2008) Microbial contributions to climate change through carbon cycle feedbacks. ISME J 2:805–814

    Article  PubMed  CAS  Google Scholar 

  59. Valiela I, Teal JM, Persson NY (1976) Production and dynamics of experimentally enriched salt marsh vegetation: belowground biomass. Limnol Oceanogr 21:245–252

    Article  Google Scholar 

  60. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol. 164:347–355

    Article  Google Scholar 

  61. Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, la Pierre K, Risch AC, Seabloom EW, Schütz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112:10967–10972

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Allison SD, Hanson CA, Treseder KK (2007) Nitrogen fertilization reduces diversity and alters community structure of active fungi in boreal ecosystems. Soil Biol Biochem 39:1878–1887

    Article  CAS  Google Scholar 

  63. Lin X, Feng Y, Zhang H, Chen R, Wang J, Zhang J, Chu H (2012) Long-term balanced fertilization decreases arbuscular mycorrhizal fungal diversity in an arable soil in North China revealed by 454 pyrosequencing. Environ Sci Technol 46:5764–5771

    Article  PubMed  CAS  Google Scholar 

  64. Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115

    Article  Google Scholar 

  65. v Wintzingerode F, Göbel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol. Rev. 21:213–229

    Article  CAS  Google Scholar 

  66. Zheng Y, Chen L, Luo C-Y et al (2016) Plant identity exerts stronger effect than fertilization on soil arbuscular mycorrhizal fungi in a sown pasture. Microb Ecol 72:647–658

    Article  PubMed  CAS  Google Scholar 

  67. Zhou J, Jiang X, Zhou B, Zhao B, Ma M, Guan D, Li J, Chen S, Cao F, Shen D, Qin J (2016) Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem 95:135–143

    Article  CAS  Google Scholar 

  68. Torta L, Lo Piccolo S, Piazza G, Burruano S, Colombo P, Ottonello D, Perrone R, di Maida G, Pirrotta M, Tomasello A, Calvo S (2015) Lulwoana sp., a dark septate endophyte in roots of Posidonia oceanica (L.) Delile seagrass. Plant Biol. 17:505–511

    Article  PubMed  CAS  Google Scholar 

  69. Borer ET, Seabloom EW, Gruner DS, Harpole WS, Hillebrand H, Lind EM, Adler PB, Alberti J, Anderson TM, Bakker JD, Biederman L, Blumenthal D, Brown CS, Brudvig LA, Buckley YM, Cadotte M, Chu C, Cleland EE, Crawley MJ, Daleo P, Damschen EI, Davies KF, DeCrappeo NM, du G, Firn J, Hautier Y, Heckman RW, Hector A, HilleRisLambers J, Iribarne O, Klein JA, Knops JMH, la Pierre KJ, Leakey ADB, Li W, MacDougall AS, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Mortensen B, O'Halloran LR, Orrock JL, Pascual J, Prober SM, Pyke DA, Risch AC, Schuetz M, Smith MD, Stevens CJ, Sullivan LL, Williams RJ, Wragg PD, Wright JP, Yang LH (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature 508:517–520

    Article  PubMed  CAS  Google Scholar 

  70. De Filippis F, Laiola M, Blaiotta G, Ercolini D (2017) Different amplicon targets for sequencing-based studies of fungal diversity. Appl. Environ. Microbiol. 83:e00905–e00917

    Article  PubMed  PubMed Central  Google Scholar 

  71. Averill C, Waring B (2018) Nitrogen limitation of decomposition and decay: how can it occur? Glob. Chang. Biol. 24:1417–1427

    Article  PubMed  Google Scholar 

  72. Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257

    Article  Google Scholar 

  73. Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol. Lett. 13:819–828

    Article  PubMed  Google Scholar 

  74. Henriksen TM, Breland TA (1999) Nitrogen availability effects on carbon mineralization, fungal and bacterial growth, and enzyme activities during decomposition of wheat straw in soil. Soil Biol Biochem 31:1121–1134

    Article  CAS  Google Scholar 

  75. van Diepen LTA, Frey SD, Landis EA, Morrison EW, Pringle A (2017) Fungi exposed to chronic nitrogen enrichment are less able to decay leaf litter. Ecology 98:5–11

    Article  PubMed  Google Scholar 

  76. Fox L, Valiela I, Kinney EL (2012) Vegetation cover and elevation in long-term experimental nutrient-enrichment plots in great Sippewissett Salt Marsh, Cape Cod, Massachusetts: implications for eutrophication and sea level rise. Estuar. Coasts 35:445–458

    Article  CAS  Google Scholar 

  77. Peng X, Ji Q, Angell JH, Kearns PJ, Yang HJ, Bowen JL, Ward BB (2016) Long-term fertilization alters the relative importance of nitrate reduction pathways in salt marsh sediments. J Geophys Res Biogeosci 121:2082–2095

    Article  CAS  Google Scholar 

  78. Hamersley MR, Howes BL (2005) Coupled nitrification-denitrification measured in situ in a Spartina alterniflora marsh with a 15NH4 + tracer. Mar Ecol Prog Ser 299:123–135

    Article  CAS  Google Scholar 

  79. Shoun H, Fushinobu S, Jiang L, Kim SW, Wakagi T (2012) Fungal denitrification and nitric oxide reductase cytochrome P450nor. Philos Trans R Soc Lond B Biol Sci 367:1186–1194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Belser LW (1977) Nitrate reduction to nitrite, a possible source of nitrite for growth of nitrite-oxidizing bacteria. Appl. Environ. Microbiol. 34:403–410

    PubMed  PubMed Central  CAS  Google Scholar 

  81. Ravishankara a R, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

    Article  PubMed  CAS  Google Scholar 

  82. Roco CA, Bergaust LL, Bakken LR, Yavitt JB, Shapleigh JP (2017) Modularity of nitrogen-oxide reducing soil bacteria: linking phenotype to genotype. Environ. Microbiol. 19:2507–2519

    Article  PubMed  CAS  Google Scholar 

  83. Kearns PJ, Angell JH, Feinman SG, Bowen JL (2015) Long-term nutrient addition differentially alters community composition and diversity of genes that control nitrous oxide flux from salt marsh sediments. Estuar. Coast. Shelf Sci. 154:39–47

    Article  CAS  Google Scholar 

  84. Moseman-Valtierra S, Gonzalez R, Kroeger KD, Tang J, Chao WC, Crusius J, Bratton J, Green A, Shelton J (2011) Short-term nitrogen additions can shift a coastal wetland from a sink to a source of N2O. Atmos. Environ. 45:4390–4397

    Article  CAS  Google Scholar 

  85. Kenny C, Yamulki S, Blackwell M, Maltby E, French P, Birgand F (2005) The release of nitrous oxide from the intertidal zones of two European estuaries in response to increased ammonium and nitrate loading. Water Air Soil Pollut Focus 4:61–66

    Article  CAS  Google Scholar 

  86. Hirota M, Senga Y, Seike Y, Nohara S, Kunii H (2007) Fluxes of carbon dioxide, methane and nitrous oxide in two contrastive fringing zones of coastal lagoon, Lake Nakaumi, Japan. Chemosphere 68:597–603

    Article  PubMed  CAS  Google Scholar 

  87. Ji Q, Babbin AR, Peng X, Bowen JL, Ward BB (2015) Nitrogen substrate-dependent nitrous oxide cycling in salt marsh sediments. J. Mar. Res. 73:71–92

    Article  CAS  Google Scholar 

  88. Middelburg JJ, Klaver G, Nieuwenhuize J, Markusse RM, Vlug T, van der Nat FJWA (1995) Nitrous oxide emissions from estuarine intertidal sediments. Hydrobiologia 311:43–55

    Article  CAS  Google Scholar 

  89. Kristensen E, Ahmed SI, Devol AH (1995) Aerobic and anaerobic decomposition of organic matter in marine sediment: which is fastest? Limnol Oceanogr 40:1430–1437

    Article  CAS  Google Scholar 

  90. Solomon D, Lehmann J, Kinyangi J (2007) Long-term impacts of anthropogenic perturbations on dynamics and speciation of organic carbon in tropical forest and subtropical grassland ecosystems. Glob Chang Biol

  91. Ekschmitt K, Kandeler E, Poll C, Brune A, Buscot F, Friedrich M, Gleixner G, Hartmann A, Kästner M, Marhan S, Miltner A, Scheu S, Wolters V (2008) Soil-carbon preservation through habitat constraints and biological limitations on decomposer activity. J Plant Nutr Soil Sci. 171:27–35

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank researchers of the TIDE Project (NSF DEB 0924287, DEB 0923689, DEB 0213767, DEB 1354494, DEB 1353140, and DEB 1719621) for maintaining the site and nutrient enrichment experiment. We would also like to thank Sarah Feinman and members of the Bowen lab for their help in field collections. FT-IR analysis was performed at the Woods Hole Research Center in the lab of Jonathan Sanderman. Additional support was received from the Plum Island LTER (NSF OCE 1673630, 0423565, 1058747). All sequence data from this study is available in the Sequence Read Archive under accession number SRP100756.

Funding

This work was funded by the NSF awards DEB 1350491 and DEB 1353140 to JLB and an NSF Research Experience for Undergraduates Award DBI-1359241 to Dr. Rachel Skvirsky.

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Correspondence to Jennifer L. Bowen.

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Kearns, P.J., Bulseco-McKim, A.N., Hoyt, H. et al. Nutrient Enrichment Alters Salt Marsh Fungal Communities and Promotes Putative Fungal Denitrifiers. Microb Ecol 77, 358–369 (2019). https://doi.org/10.1007/s00248-018-1223-z

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Keywords

  • Salt marsh
  • Fungal ecology
  • Fungal denitrification
  • Nutrient enrichment
  • Decomposition