Abstract
Boreal forest encompasses approximately 30% of the terrestrial carbon (C) storage, representing an important hotspot of C transformations mediated by soil microbial communities in the changing environment. However, our understanding of the microbial community characteristics and the core components of soil microbiome in different succession scenarios of boreal forest is still limited. Here, we compared the diversity, activities and community composition of both bacteria and fungi between upland and swamp boreal forest soils. The microbial diversity and activity were remarkably lower in swamp than upland soils. The bacterial and fungal community compositions were significantly different between the swamp and upland soils. Linear Discriminant Analysis Effect Size analysis identified Firmicutes and Ascomycota as molecular markers for the swamp while Actinobacteria and Mucoromycotina for the upland. Molecular ecological networks revealed significantly less modules and putative keystone species of bacteria and fungi in swamp than in upland soils. The differences in soil microbiome profiles between the swamp and upland sites of boreal forest were attributed to soil moisture content, soil pH and nutrients. Our results suggested that the soil microbial community composition and structure significantly changed across the different succession stages of the boreal forest biome.
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Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M (2008) Computing topological parameters of biological networks. Bioinformatics 24:282–284
Awasthi A, Singh M, Soni SK, Singh R, Kalra A (2014) Biodiversity acts as insurance of productivity of bacterial communities under abiotic perturbations. The ISME Journal 8:2445–2452
Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, Žifčáková L, Šnajdr J, Rídl J, Vlček Č (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. The ISME Journal 6:248–258
Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press
Barreto CR, Morrissey EM, Wykoff D, Chapman SK (2018) Co-occurring mangroves and salt marshes differ in microbial community composition. Wetlands 1:1–12
Berry D, Widder S (2014) Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Frontiers in Microbiology 5:1–14
Bontemps C, Elliott G, Simon M, Dos Reis F, Gross E, Lawton R, Neto N, Loureiro M, De Faria S, Sprent J (2010) Burkholderia species are ancient symbionts of legumes. Molecular Ecology 19:44–52
Cai F, Pang G, Miao Y, Li R, Li R, Shen Q, Chen W (2017) The nutrient preference of plants influences their rhizosphere microbiome. Applied Soil Ecology 110:146–150
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:335–336
Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Applied and Environemntal Microbiology 76:999–1007
Cheung GW, Lau RS (2008) Testing mediation and suppression effects of latent variables: bootstrapping with structural equation models. Organizational Research Methods 11:296–325
Clemmensen K, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay R, Wardle D, Lindahl B (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods 10:996–998
Faust K, Raes J (2012) Microbial interactions: from networks to models. Nature Reviews. Microbiology 10:538–550
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, Huttenhower C (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Computational Biology 8:e1002606
Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology 71:4117–4120
Ghoul M, Mitri S (2016) The ecology and evolution of microbial competition. Trends in Microbiology 24:833–845
Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-De LSP, Gross E, Dos Reis FB, Sprent JI (2011) Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Molecular Plant-Microbe Interactions 24:1276–1288
Hasselquist NJ, Metcalfe DB, Inselsbacher E, Stangl Z, Oren R, Näsholm T, Högberg P (2016) Greater carbon allocation to mycorrhizal fungi reduces tree nitrogen uptake in a boreal forest. Ecology 97:1012–1022
Högberg MN, Högberg P, Myrold DD (2007) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–601
Hu HW, Chen D, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiology Review 39:729–749
Hu HW, Trivedi P, He JZ, Singh BK (2017) Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation. Environmental Microbiology 19:4808–4828
Jaatinen K, Laiho R, Vuorenmaa A, del Castillo U, Minkkinen K, Pennanen T, Penttilä T, Fritze H (2008) Responses of aerobic microbial communities and soil respiration to water-level drawdown in a northern boreal fen. Environmental Microbiology 10:339–353
Jackson CR, Liew KC, Yule CM (2009) Structural and functional changes with depth in microbial communities in a tropical Malaysian peat swamp forest. Microbial Ecology 57:402–412
Jones MC, Harden J, O'donnell J, Manies K, Jorgenson T, Treat C, Ewing S (2017) Rapid carbon loss and slow recovery following permafrost thaw in boreal peatlands. Global Change Biology 23:1109–1127
Kanokratana P, Uengwetwanit T, Rattanachomsri U, Bunterngsook B, Nimchua T, Tangphatsornruang S, Plengvidhya V, Champreda V, Eurwilaichitr L (2011) Insights into the phylogeny and metabolic potential of a primary tropical peat swamp forest microbial community by metagenomic 501 analysis. Microbial Ecology 61:518–528
Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JM (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proceedings of the National Academy of Sciences of the United States of America 112:10967–10972
Li J, Zheng YM, Liu YR, Ma YB, Hu HW, He JZ (2014) Initial copper stress strengthens the resistance of soil microorganisms to a subsequent copper stress. Microbial Ecology 67:931–941
Li J, Ma YB, Hu HW, Wang JT, Liu YR, He JZ (2015a) Field-based evidence for consistent responses of bacterial communities to copper contamination in two contrasting agricultural soils. Frontiers in Microbiology 6:31
Li J, JT W, Hu HW, Ma YB, Zhang LM, He JZ (2015b) Copper pollution decreases the resistance of soil microbial community to subsequent dry–rewetting disturbance. Journal of Environmental Sciences 39:155–164
Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi–potential organic matter decomposers, yet not saprotrophs. The New Phytologist 205:1443–1447
Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. The New Phytologist 173:611–620
Lodge DJ, Padamsee M, Matheny PB, Aime MC, Cantrell SA, Boertmann D, Kovalenko A, Vizzini A, Dentinger BTM, Kirk PM (2014) Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales). Fungal Diversity 64:1–99
Luyssaert S, Janssens IA, Sulkava M, Papale D, Dolman AJ, Reichstein M, Hollmén J, Martin JG, Suni T, Vesala T (2007) Photosynthesis drives anomalies in net carbon-exchange of pine forests at different latitudes. Global Change Biology 13:2110–2127
Ma B, Wang HZ, Dsouza M, Lou J, He Y, Dai ZM, Brookes PC, Xu JM, Gilbert JA (2016) Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in eastern China. The ISME Journal 10:1891–1901
Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecological Monographs 80:89–106
Mélida H, Sain D, Stajich JE, Bulone V (2015) Deciphering the uniqueness of Mucoromycotina cell walls by combining biochemical and phylogenomic approaches. Environmental Microbiology 17:1649–1662
Mougi A, Kondoh M (2012) Diversity of interaction types and ecological community stability. Science 337:349–351
Pan Y, Birdsey RA, Fang J, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Reich PB (2012) Key canopy traits drive forest productivity. Proceedings of the National Academy of Sciences of the United States of America 279:2128–2134
Price DT, Alfaro RI, Brown KJ, Flannigan MD, Fleming RA, Hogg EH, Girardin MP, Lakusta T, Johnston M, McKenney DW, Pedlar JH, Stratton T, Sturrock RN, Thompson ID, Trofymow JA, Venierc LA (2013) Anticipating the consequences of climate change for Canada’s 70 boreal forest ecosystems. Environmental Reviews 21:322–365
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41:D590–D596
Rosling A, Timling I, Taylor DL (2013) Archaeorhizomycetes: Patterns of Distribution and Abundance in Soil. Springer Berlin Heidelberg
Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. The ISME Journal 4:1340–1351
Saavedra S, Stouffer DB, Uzzi B, Bascompte J (2011) Strong contributors to network persistence are the most vulnerable to extinction. Nature 478:233–235
Schmidt S, Costello E, Nemergut D, Cleveland CC, Reed S, Weintraub M, Meyer A, Martin A (2007) Biogeochemical consequences of rapid microbial turnover and seasonal succession in soil. Ecology 88:1379–1385
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biology 12:R60
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Research 13:2498–2504
Singh BK, Bardgett RD, Smith P, Reay DS (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nature Reviews. Microbiology 8:779–790
Soffer N, Zaneveld J, Vega Thurber R (2015) Phage–bacteria network analysis and its implication for the understanding of coral disease. Environmental Microbiology 17:1203–1218
Srinivasan S, Hoffman NG, Morgan MT, Matsen FA, Fiedler TL, Hall RW, Ross FJ, Mccoy CO, Bumgarner R, Marrazzo JM (2012) Bacterial communities in women with bacterial vaginosis: high resolution phylogenetic analyses reveal relationships of microbiota to clinical criteria. PLoS One 7:e37818
Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiology Ecology 80:735–746
Suzuki MT, Taylor LT, Delong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Applied and Environmental Microbiology 66:4605–4614
Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Gurvan M (2011) Environmental and gut Bacteroidetes: the food connection. Frontiers in Microbiology 2:1–16
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 Biology & Biochemistry 84:53–64
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology 73:5261–5267
Wang JT, Zheng YM, Hu HW, Li J, Zhang LM, Chen BD, Chen WP, He JZ (2016) Coupling of soil prokaryotic diversity and plant diversity across latitudinal forest ecosystems. Scientific Reports 6:19561
Wang S, Wang XB, Han XG, Deng Y (2018) Higher precipitation strengthens the microbial interactions in semi-arid grassland soils. Global Ecology and Biogeography 27:570–580. https://doi.org/10.1111/geb.12718
Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Applied and Environmental Microbiology 75:2046–2056
Wu J, Joergensen R, Pommerening B, Chaussod R, Brookes P (1990) Measurement of soil microbial biomass C by fumigation-extraction - an automated procedure. Soil Biology and Biochemistry 22:1167–1169
Yabe S, Sakai Y, Abe K, Yokota A (2017) Diversity ofKtedonobacteriawith Actinomycetes-like morphology in terrestrial environments. Microbes and Environments 32:61–70
Zhang Y, Schoch CL, Fournier J, Crous PW, de Gruyter J, Woudenberg JHC, Hirayama K, Tanaka K, Pointing SB, Spatafora JW, Hyde KD (2009) Multi-locus phylogeny of Pleosporales: a taxonomic, ecological and evolutionary re-evaluation. Studies in Mycology 64:85–102
Žifčáková L, Větrovský T, Howe A, Baldrian P (2016) Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environmental Microbiology 18:288–301
Acknowledgements
This work was funded by Fundamental Research Funds for the Central Non-profit Research Institution of Chinese Academy of Forestry (CAFYBB2016QA020) and National Natural Science Foundation of China (No. 41601577). We thank Dr. Zongming Li for his generous help in edaphic property analysis. We are also grateful for proofreading of the paper by Dr. Phillip Chalk.
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Li, J., Hu, HW., Cai, ZJ. et al. Contrasting Soil Bacterial and Fungal Communities between the Swamp and Upland in the Boreal Forest and their Biogeographic Distribution Patterns. Wetlands 39, 441–451 (2019). https://doi.org/10.1007/s13157-018-1086-6
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DOI: https://doi.org/10.1007/s13157-018-1086-6