Many of the world's peatlands have been affected by water table drawdown and subsequent loss of organic matter. Rewetting has been proposed as a measure to restore peatland functioning and to halt carbon loss, but its effectiveness is subject to debate. An important prerequisite for peatland recovery is a return of typical microbial communities, which drive key processes. To evaluate the effect of rewetting, we investigated 13 fen peatland areas across a wide (>1500 km) longitudinal gradient in Europe, in which we compared microbial communities between drained, undrained, and rewetted sites. There was a clear difference in microbial communities between drained and undrained fens, regardless of location. Community recovery upon rewetting was substantial in the majority of sites, and predictive functional profiling suggested a concomitant recovery of biogeochemical peatland functioning. However, communities in rewetted sites were only similar to those of undrained sites when soil organic matter quality (as expressed by cellulose fractions) and quantity were still sufficiently high. We estimate that a minimum organic matter content of ca. 70% is required to enable microbial recovery. We conclude that peatland recovery after rewetting is conditional on the level of drainage-induced degradation: severely altered physicochemical peat properties may preclude complete recovery for decades.

B WARE Research Centre Toernooiveld 1 6525 ED Nijmegen The Netherlands

Biology Centre of the Czech Academy of Sciences Institute of Soil Biology and SoWa RI Na Sádkách 7 CZ 37005 České Budějovice Czech Republic

Charles University Institute for Environmental Studies Benátská 2 CZ 128282801 Prague Czech Republic

Department of Plant Ecology and Environmental Conservation Faculty of Biology University of Warsaw Centre for Biological and Chemical Sciences ul Żwirki i Wigury 101 02 089 Warszawa Poland

Ecosystem Management Research Group Department of Biology University of Antwerp Universiteitsplein 1C 2610 Wilrijk Belgium

Institute of Botany and Landscape Ecology University of Greifswald partner in the Greifswald Mire Centre Soldmannstr 15 17489 Greifswald Germany

KWR Watercycle Research Institute P O Box 1072 3430 BB Nieuwegein The Netherlands

Plants and Ecosystems Research Group Department of Biology University of Antwerp Universiteitsplein 1C 2610 Wilrijk Belgium

Soil Quality and Climate Change Division for Environment and Natural Resources Norwegian Institute of Bioeconomy Research Hogskoleveien 7 1430 Aas Norway

See more in PubMed

Gorham E. Northern peatlands: role in the carbon cycle and probable responses to climatic warming. Ecol Appl. 1991;1:182–95. PubMed

Yu Z. Northern peatland carbon stocks and dynamics: a review. Biogeosciences. 2012;9:4071–85.

Knox SH, Sturtevant C, Matthes JH, Koteen L, Verfaillie J, Baldocchi D. Agricultural peatland restoration: effects of land-use change on greenhouse gas (CO2 and CH4) fluxes in the Sacramento-San Joaquin Delta. Glob Change Biol. 2015;21:750–65. PubMed

Fenner N, Freeman C. Drought-induced carbon loss in peatlands. Nat Geosci. 2011;4:895–900.

Freeman C, Ostle N, Kang H. An enzymic ‘latch’ on a global carbon store - a shortage of oxygen locks up carbon in peatlands by restraining a single enzyme. Nature. 2001;409:149. PubMed

Kwon MJ, Haraguchi A, Kang H. Long-term water regime differentiates changes in decomposition and microbial properties in tropical peat soils exposed to the short-term drought. Soil Biol Biochem. 2013;60:33–44.

Laine J, Vasander H, Sallantaus T. Ecological effects of peatland drainage for forestry. Environ Rev. 1995;3:286–303.

Minayeva TY, Bragg O, Sirin A. Towards ecosystem-based restoration of peatland biodiversity. Mires Peat. 2017;19:1–36.

Mälson K, Backéus I, Rydin H. Long-term effects of drainage and initial effects of hydrological restoration on rich fen vegetation. Appl Veg Sci. 2007;11:99–106.

Juottonen H, Hynninen A, Nieminen M, Tuomivirta TT, Tuittila ES, Nousiainen H, et al. Methane-cycling microbial communities and methane emission in natural and restored peatlands. Appl Environ Micro. 2012;78:6386–9. PubMed PMC

Lamers LP, Vile MA, Grootjans AP, Acreman MC, van Diggelen R, Evans MG, et al. Ecological restoration of rich fens in Europe and North America: from trial and error to an evidence‐based approach. Biol Rev. 2015;90:182–203. PubMed

Joosten H. The Global Peatland CO2 Picture: peatland status and drainage related emissions in all countries of the world. Ede: Wetlands International; 2009.

Bardgett RD, Van Der Putten WH. Belowground biodiversity and ecosystem functioning. Nature. 2014;515:505. PubMed

Andersen R, Francez A-J, Rochefort L. The physicochemical and microbiological status of a restored bog in Québec: Identification of relevant criteria to monitor success. Soil Biol Biochem. 2006;38:1375–87.

Putkinen A, Tuittila E-S, Siljanen HM, Bodrossy L, Fritze H. Recovery of methane turnover and the associated microbial communities in restored cutover peatlands is strongly linked with increasing Sphagnum abundance. Soil Biol Biochem. 2018;116:110–9.

Wen X, Unger V, Jurasinski G, Koebsch F, Horn F, Rehder G, et al. Predominance of methanogens over methanotrophs in rewetted fens characterized by high methane emissions. Biogeosciences. 2018;15:6519–36.

Potter C, Freeman C, Golyshin PN, Ackermann G, Fenner N, McDonald JE, et al. Subtle shifts in microbial communities occur alongside the release of carbon induced by drought and rewetting in contrasting peatland ecosystems. Sci Rep. 2017;7:11314. PubMed PMC

Sinsabaugh RL, Hill BH, Shah JJF. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature. 2009;462:795–U117. PubMed

Larmola T, Leppänen SM, Tuittila E-S, Aarva M, Merilä P, Fritze H, et al. Methanotrophy induces nitrogen fixation during peatland development. PNAS. 2014;111:734–9. PubMed PMC

Liebner S, Zeyer J, Wagner D, Schubert C, Pfeiffer EM, Knoblauch C. Methane oxidation associated with submerged brown mosses reduces methane emissions from Siberian polygonal tundra. J Ecol. 2011;99:914–22.

Aggenbach CJ, Backx H, Emsens WJ, Grootjans AP, Lamers LP, Smolders AJ, et al. Do high iron concentrations in rewetted rich fens hamper restoration. Preslia. 2013;85:405–20.

Myers B, Webster KL, Mclaughlin JW, Basiliko N. Microbial activity across a boreal peatland nutrient gradient: the role of fungi and bacteria. Wetl Ecol Manag. 2012;20:77–88.

Ellenberg H, Leuschner C. Vegetation Mitteleuropas mit den Alpen: in ökologischer, dynamischer und historischer Sicht. Stuttgart: Ulmer Verlag; 2010. Vol. 8104.

Schaffers AP, Sýkora KV. Reliability of Ellenberg indicator values for moisture, nitrogen and soil reaction: a comparison with field measurements. J Veg Sci. 2000;11:225–44.

Rowland A, Roberts J. Lignin and cellulose fractionation in decomposition studies using acid‐detergent fibre methods. Commun Soil Sci Plan. 1994;25:269–77.

Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS. 2011;108:4516–22. PubMed PMC

Frostegard A, Baath E. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fert Soils. 1996;22:59–65.

Oravecz O, Elhottová D, Krištůfek V, Šustr V, Frouz J, Tříska J, et al. Application of ARDRA and PLFA analysis in characterizing the bacterial communities of the food, gut and excrement of saprophagous larvae ofPenthetria holosericea (Diptera: Bibionidae): a pilot study. Folia microbiologica. 2004;49:83. PubMed

Šnajdr J, Valášková V, Merhautová V, Cajthaml T, Baldrian P. Activity and spatial distribution of lignocellulose-degrading enzymes during forest soil colonization by saprotrophic basidiomycetes. Enzym Micro Tech. 2008;43:186–92.

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996. PubMed

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6. PubMed PMC

Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol. 2013;31:814. PubMed PMC

Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM et al. PICRUSt2: an improved and extensible approach for metagenome inference. 2019. https://www.biorxiv.org/content/10.1101/672295v1. DOI

Luton PE, Wayne JM, Sharp RJ, Riley PW. The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology. 2002;148:3521–30. PubMed

Galand PE, Saarnio S, Fritze H, Yrjälä K. Depth related diversity of methanogen Archaea in Finnish oligotrophic fen. FEMS Microbiol Ecol. 2002;42:441–9. PubMed

Lüdemann H, Arth I, Liesack W. Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Appl Environ Microbiol. 2000;66:754–62. PubMed PMC

Andersen R, Chapman SJ, Artz RRE. Microbial communities in natural and disturbed peatlands: a review. Soil Biol Biochem. 2013;57:979–94.

Morales SE, Mouser PJ, Ward N, Hudman SP, Gotelli NJ, Ross DS, et al. Comparison of bacterial communities in New England Sphagnum bogs using terminal restriction fragment length polymorphism (T-RFLP) Micro Ecol. 2006;52:34–44. PubMed

Eilers KG, Debenport S, Anderson S, Fierer N. Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem. 2012;50:58–65.

Jackson CR, Liew KC, Yule CM. Structural and functional changes with depth in microbial communities in a tropical malaysian peat swamp forest. Micro Ecol. 2009;57:402–12. PubMed

Brune A, Frenzel P, Cypionka H. Life at the oxic–anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev. 2000;24:691–710. PubMed

Basiliko N, Henry K, Gupta V, Moore T, Driscoll B, Dunfield P. Controls on bacterial and archaeal community structure and greenhouse gas production in natural, mined, and restored Canadian peatlands. Front Microbiol. 2013;4:215. PubMed PMC

Hooijer A, Page S, Jauhiainen J, Lee WA, Lu XX, Idris A, et al. Subsidence and carbon loss in drained tropical peatlands. Biogeosciences. 2012;9:1053–71.

Minkkinen K, Laine J. Effect of forest drainage on the peat bulk density of pine mires in Finland. Can J For Res. 1998;28:178–86.

Pérez J, Munoz-Dorado J, De la Rubia T, Martinez J. Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol. 2002;5:53–63. PubMed

Borren W, Bleuten W, Lapshina ED. Holocene peat and carbon accumulation rates in the southern taiga of western Siberia. Quat Res. 2004;61:42–51.

Succow M, Joosten H. landschaftsökologische Moorkunde. Stuttgart: E. Schweizerbart’sche Verlagsbuchhandlung; 2012.

Raghoebarsing AA, Smolders AJ, Schmid MC, Rijpstra WIC, Wolters-Arts M, Derksen J, et al. Methanotrophic symbionts provide carbon for photosynthesis in peat bogs. Nature. 2005;436:1153. PubMed

Eilers KG, Lauber CL, Knight R, Fierer N. Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biol Biochem. 2010;42:896–903.

Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR. Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry. 2007;82:229–40.

Hiraishi T, Krug T, Tanabe K, Srivastava N, Baasansuren J, Fukuda M et al. 2013 supplement to the 2006 IPCC guidelines for national greenhouse gas inventories: Wetlands. Switzerland: IPCC; 2014.