Marine-to-terrestrial transition represents one of the most fundamental shifts in microbial life. Understanding the distribution and drivers of soil microbial communities across coastal ecosystems is critical given the roles of microbes in soil biogeochemistry and their multifaceted influence on landscape succession. Here, we studied the fungal community dynamics in a well-established salt marsh chronosequence that spans over a century of ecosystem development. We focussed on providing high-resolution assessments of community composition, diversity and ecophysiological shifts that yielded patterns of ecological succession through soil formation. Notably, despite containing 10- to 100-fold lower fungal internal transcribed spacer abundances, early-successional sites revealed fungal richnesses comparable to those of more mature soils. These newly formed sites also exhibited significant temporal variations in β-diversity that may be attributed to the highly dynamic nature of the system imposed by the tidal regime. The fungal community compositions and ecophysiological assignments changed substantially along the successional gradient, revealing a clear signature of ecological replacement and gradually transforming the environment from a marine into a terrestrial system. Moreover, distance-based linear modelling revealed soil physical structure and organic matter to be the best predictors of the shifts in fungal β-diversity along the chronosequence. Taken together, our study lays the basis for a better understanding of the spatiotemporally determined fungal community dynamics in salt marshes and highlights their ecophysiological traits and adaptation in an evolving ecosystem.

Genomics and Computational Biology Group CPqRR FIOCRUZ Belo Horizonte MG Brazil

Laboratory of Environmental Microbiology Institute of Microbiology of the Czech Academy of Sciences Prague Czech Republic

Microbial Ecology Group Genomic Research in Ecology and Evolution in Nature University of Groningen Groningen The Netherlands

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Abarenkov K, Henrik Nilsson R, Larsson KH, Alexander IJ, Eberhardt U, Erland S et al. (2010). The UNITE database for molecular identification of fungi – recent updates and future perspectives. New Phytol 186: 281–285. PubMed

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

Bakker JP. (2014) Ecology of Salt Marshes: 40 Years of Research in the Wadden Sea. Wadden Academy Ruiterskwartier: Leeuwarden, The Netherlands.

Bakker JP, Esselink P, van der Wal R, Dijkema KS. (1997). Options for restoration and management of coastal salt marshes in Europe. In: Urbanska KM, Webb NR, Edwards PJ (eds), Restoration Ecology and Sustainable Development. Cambridge University Press: Cambridge, UK, pp 286–322.

Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T et al. (2012). Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6: 248–258. PubMed PMC

Baldrian P, Trögl J, Frouz J, Šnajdr J, Valášková V, Merhautová V et al. (2008). Enzyme activities and microbial biomass in topsoil layer during spontaneous succession in spoil heaps after brown coal mining. Soil Biol Biochem 40: 2107–2115.

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

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: 189. PubMed PMC

Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A 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.

Blaalid R, Carlsen T, Kumar S, Halvorsen R, Ugland KI, Fontana G et al. (2012). Changes in the root-associated fungal communities along a primary succession gradient analysed by 454 pyrosequencing. Mol Ecol 21: 1897–1908. PubMed

Brown SP, Jumpponen A. (2014). Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. Mol Ecol 23: 481–497. PubMed

Buchan A, Newell SY, Moreta JI, Moran MA. (2002). Analysis of internal transcribed spacer (ITS) regions of rRNA genes in fungal communities in a southeastern U.S. salt marsh. Microb Ecol 43: 329–340. PubMed

Burke DJ, Hamerlynck EP, Hahn D. (2002). Interactions among plant species and microorganisms in salt marsh sediments. Appl Environ Microbiol 68: 1157–1164. PubMed PMC

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336. PubMed PMC

Chapin FS, McFarland J, McGuire AD, Euskirchen ES, Ruess RW, Kielland K. (2009). The changing global carbon cycle: linking plant-soil carbon dynamics to global consequences. J Ecol 97: 840–850.

Chmura GL, Anisfeld SC, Cahoon DR, Lynch JC. (2003). Global carbon sequestration in tidal, saline wetland soils. Glob Biogeochem Cy 17: 1111–1133.

Corsaro D, Walochnik J, Venditti D, Steinmann J, Müller KD, Michel R. (2014). Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. Parasitol Res 113: 1909–1918. PubMed

Crowther TW, Boddy L, Hefin Jones T. (2012). Functional and ecological consequences of saprotrophic fungus–grazer interactions. ISME J 6: 1992–2001. PubMed PMC

Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S et al. (2012). Coastal eutrophication as a driver of salt marsh loss. Nature 490: 388–392. PubMed

Dini-Andreote F, Pereira e Silva MC, Triadó-Margarit X, Casamayor EO, van Elsas JD, Salles JF. (2014). Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning. ISME J 8: 1989–2001. PubMed PMC

Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF. (2015). Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA 112: E1326–E1332. PubMed PMC

Druva-Lusite I, Ievinsh G. (2010). Diversity of arbuscular mycorrhizal symbiosis in plants from coastal habitats. Environ Exp Biol 8: 17–34.

Edgar RC. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10: 996–998. PubMed

Fierer N, Bradford MA, Jackson RB. (2007). Toward an ecological classification of soil bacteria. Ecology 88: 1354–1364. PubMed

Fierer N, Jackson RB. (2006). The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103: 626–631. PubMed PMC

Fierer N, Nemergut D, Knight R, Craine JM. (2010). Changes through time: integrating microorganisms into the study of succession. Res Microbiol 161: 635–642. PubMed

Gardes M, Bruns TD. (1993). ITS primers with enhanced specificity for basidiomycetes –application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113–118. PubMed

Hartmann A, Schmid M, van Tuinen D, Berg G. (2009). Plant-driven selection of microbes. Plant Soil 321: 235–257.

Heimann M, Reichstein M. (2008). Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451: 289–292. PubMed

Heinemeyer A, Hartley IP, Evans SP, De la Fuente JAC, Ineson P. (2007). Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas. Glob Change Biol 13: 1786–1797.

Hildebrandt U, Janetta K, Ouziad F, Renne B, Nawrath K, Bothe H. (2001). Arbuscular mycorrhizal colonization of halophytes in Central European salt marshes. Mycorrhiza 10: 175–183.

Högberg P, Nordgren A, Buchmann N, Taylor AF, Ekblad A, Högberg MN et al. (2001). Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411: 789–792. PubMed

James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ et al. (2006. a). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818–822. PubMed

James TY, Letcher PM, Longcore JE, Mozley-Standridge PD, Powell MJ, Griffith GW et al. (2006. b). A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota). Mycologia 98: 860–871. PubMed

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

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

Legendre P, Anderson M. (1999). Distance-based redundancy analyses: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69: 1–24.

Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R et al. (2013). Fungal community analysis by high-throughput sequencing of amplified markers — a user's guide. New Phytol 199: 288–299. PubMed PMC

Longo AV, Rodriguez D, da Silva Leite D, Toledo LF, Almeralla CM, Burrowes PA et al. (2013). ITS1 copy number varies among Batrachochytrium dendrobatidis strains: implications for qPCR estimates of infection intensity from field-collected amphibian skin swabs. PLoS One 8: e59499. PubMed PMC

McArdle B, Anderson M. (2001). Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290–297.

McGuire KL, Treseder KK. (2010). Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42: 529–535.

Meyling NV, Eilenberg J. (2007). Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43: 145–155.

Millard P, Singh B. (2010). Does grassland vegetation drive soil microbial diversity? Nutr Cycl Agroecosys 88: 147–158.

Mohamed DJ, Martiny JBH. (2011). Patterns of fungal diversity and composition along a salinity gradient. ISME J 5: 379–388. PubMed PMC

Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A et al. (2007). Microbial community succession in an unvegetated, recently deglaciated soil. Microbiol Ecol 53: 110–122. PubMed

Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J. (1999). Ecosystem properties and microbial community changes in primary succession on a glacier foreland. Oecologia 119: 239–246. PubMed

Olff H, de Leeuw J, Bakker JP, Platerink RJ, van Wijnen HJ. (1997). Vegetation succession and herbivory in a salt marsh: changes induced by sea level rise and silt deposition along an elevational gradient. J Ecol 85: 799–814.

Pylro VS, Roesch LF, Ortega JM, do Amaral AM, Tótola MR, Hirsch PR et al. (2014). Brazilian microbiome project: revealing the unexplored microbial diversity - challenges and prospects. Microb Ecol 67: 237–241. PubMed

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

Salles JF, Poly F, Schmid B, Le Roux X. (2009). Community niche predicts the functioning of denitrifying bacterial assemblages. Ecology 90: 3324–3332. PubMed

Schrama M, Berg MP, Olff H. (2012). Ecosystem assembly rules: the interplay of green and brown webs during salt marsh succession. Ecology 93: 2353–2364. PubMed

Schrama M, Jouta J, Berg MP, Olff H. (2013). Food web assembly at the landscape scale: using stable isotopes to reveal changes in trophic structure during succession. Ecosystems 16: 627–638.

Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA et al. (2011). Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci USA 109: 6241–6246. PubMed PMC

Smith DP, Peay KG. (2014). Sequence depth, not PCR replication, improves ecological inference from next generation DNA sequencing. PLoS One 9: e90234. PubMed PMC

Tedersoo L, Bahram M, Polme S, Koljalg U, Yorou NS, Wijesundera R et al. (2014). Global diversity and geography of soil fungi. Science 346: 1256688. PubMed

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. PubMed

Treseder KK, Lennon JT. (2015). Fungal traits that drive ecosystem dynamics on land. Microbiol Mol Biol Rev 79: 243–262. PubMed PMC

Urbanová M, Šnajdr J, Baldrian P. (2015). Composition of fungal and bacterial communities in forest litter and soil is largely determined by dominant trees. Soil Biol Biochem 84: 53–64.

Van Wijnen HJ, Bakker JP, de Vries Y. (1997). Twenty years of salt marsh succession on a Dutch coastal barrier island. J Coast Conservat 3: 9–18.

Větrovský T, Baldrian P. (2013). Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fert Soils 49: 1027–1037.

Větrovský T, Kolařík M, Žifčáková L, Zelenka T, Baldrian P. (2015). The rpb2 gene represents a viable alternative molecular marker for the analysis of environmental fungal communities. Mol Ecol Resour e-pub ahead of print 19 August 2015; doi: 10.1111/1755-0998.12456. PubMed

Vilgalys R, Hester M. (1990). Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172: 4238–4246. PubMed PMC

Voříšková J, Brabcová V, Cajthaml T, Baldrian P. (2014). Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201: 269–278. PubMed

Walker LR, Wardle DA. (2014). Plant succession as an integrator of contrasting ecological time scales. Trends Ecol Evol 29: 504–510. PubMed

Walker LR, Wardle DA, Bardgett RD, Clarkson BD. (2010). The use of chronosequences in studies of ecological succession and soil development. J Ecol 98: 725–736.

White TJ, Bruns TD, Lee S, Taylor J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds), PCR Protocols: A Guide to Method and Applications. Academic Press: San Diego, CA, USA, pp 315–322.

Wilde P, Manal A, Stodden M, Sieverding E, Hildebrandt U, Bothe H. (2009). Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11: 1548–1561. PubMed

Zhang NL, Xia JY, Yu XJ, Ma KP, Wan SQ. (2011). Soil microbial community changes and their linkages with ecosystem carbon exchange under asymmetrically diurnal warming. Soil Biol Biochem 43: 2053–2059.

Zinger L, Shahnavaz B, Baptist F, Geremia RA, Choler P. (2009). Microbial diversity in alpine tundra soils correlates with snow cover dynamics. ISME J 3: 850–859. PubMed

Zinger L, Lejon DPH, Baptist F, Bouasria A, Aubert S, Geremia RA et al. (2011). Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoS ONE 6: e19950. PubMed PMC