Linkage of plant and abiotic properties to the abundance and activity of N-cycling microbial communities in Tibetan permafrost-affected regions
Ammonia oxidation and denitrification are crucial for nitrogen (N) availability and nitrous oxide production in N-limited permafrost soils. However, it remains unclear about the relative roles of abiotic and biotic properties in controlling the abundance and activity of ammonia-oxidizing and denitrifying microorganisms in permafrost-affected soils.
We analysed the potential ammonia oxidation and denitrification rates (PAO and PDR), the abundance of archaeal amoA, bacterial amoA, nirK, nirS and nosZ genes, soil characteristics, climatic and plant properties across two vegetation types in Tibetan permafrost-affected soils. The relative importance of abiotic and biotic properties in driving functional N gene abundance, PAO and PDR were assessed using variation partition analysis (VPA) and random forest (RF) model.
The functional N gene abundance and PDR were lower in alpine steppe than in alpine meadow. Variations in the PAO and PDR and functional N gene abundance were mainly explained by abiotic variables such as organic carbon and total N, then by plant properties such as plant N concentration, plant species richness and productivity based on the VPA. The RF model showed that abiotic properties (e.g., precipitation) and plant properties (e.g., plant N concentration or plant productivity) predicted the PDR and the abundance of functional N genes. Both VPA and RF model showed that the PAO and PDR could be determined by the abundance of functional N genes such as archaeal amoA gene and nosZ gene, respectively.
Our study highlights that abiotic and plant properties are important predictors of the abundance and activity of ammonia-oxidizing and denitrifying communities in permafrost-affected regions, implying that plant properties, which were previously overlooked, should be incorporated into ecosystem models for improved prediction of belowground N process rates in a changing environment.
KeywordsAmmonia oxidation Ammonia-oxidizing microorganism Biogeography Denitrifiers denitrification Permafrost
We appreciate the section editor (Dr. Feike A. Dijkstra) and two anonymous reviewers for their insightful comments on an early version of this manuscript. This work was supported by the National Key Research and Development Program of China (2017YFA0604803 and 2016YFC0500701), National Natural Science Foundation of China (41877046, 41501265 and 31670482), Key Research Program of Frontier Sciences, Chinese Academy of Sciences (QYZDB-SSW-SMC049), and Chinese Academy of Sciences-Peking University Pioneer Cooperation Team.
- Attard E, Recous S, Chabbi A, De Berranger C, Guillaumaud N, Labreuche J, Philippot L, Schmid B, Leroux X (2011) Soil environmental conditions rather than denitrifier abundance and diversity drive potential denitrification after changes in land uses. Glob Chang Biol 17:1975–1989CrossRefGoogle Scholar
- Breiman L (2001) Machine learning. Random Forests 45: 5Google Scholar
- Bru D, Ramette A, Saby NP, Dequiedt S, Ranjard L, Jolivet C, Arrouays D, Philippot L (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5: 532–542Google Scholar
- Chen YL, Chen LY, Peng YF, Ding JZ, Li F, Yang GB, Kou D, Liu L, Fang K, Zhang BB, Wang J, Yang YH (2016a) Linking microbial C:N:P stoichiometry to microbial community and abiotic factors along a 3500-km grassland transect on the Tibetan Plateau. Global Ecol Biogeogr 25:1416–1427CrossRefGoogle Scholar
- Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. Methods of soil analysis part 2: Microbiological and biochemical properties. Soil Sci Soc Am J:985–1018Google Scholar
- Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809Google Scholar
- Li SD, Cheng GD (1996) Map of Frozen Ground on Qinghai-Xizang Plateau. Gansu Culture Press, LanzhouGoogle Scholar
- Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2/3:18–22Google Scholar
- Oelmann Y, Buchmann N, Gleixner G, Habekost M, Roscher C, Rosenkranz S, Schulze E, Steinbeiss S, Temperton VM, Weigelt A, Weisser WW, Wilcke W (2011) Plant diversity effects on aboveground and belowground N pools in temperate grassland ecosystems: Development in the first 5 years after establishment. Glob Biogeochem Cycles 25:415–421CrossRefGoogle Scholar
- Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Steven MHH, Wagner H (2008) vegan: Community Ecology Package. R Package version 1.15–1Google Scholar
- Pajares S, Campo J, Bohannan BJM, Etchevers JD (2018) Environmental controls on soil microbial communities in a seasonally dry tropical forest. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00342-18
- Patra AK, Abbadie L, Clays-Josserand A, Degrange V, Grayston SJ, Guillaumaud N, Loiseau P, Louault F, Mahmood S, Nazaret S, Philippot L, Poly F, Prosser JI, Le Roux X (2006) Effects of management regime and plant species on the enzyme activity and genetic structure of N-fixing, denitrifying and nitrifying bacterial communities in grassland soils. Environ Microbiol 8:1005–1016CrossRefGoogle Scholar
- Prober SM, Leff JW, Bates ST, Borer ET, Firn J, Harpole WS, Lind EM, Seabloom EW, Adler PB, Bakker JD, Cleland EE, DeCrappeo NM, DeLorenze E, Hagenah N, Hautier Y, Hofmockel KS, Kirkman KP, Knops JMH, La Pierre KJ, MacDougall AS, McCulley RL, Mitchell CE, Risch AC, Schuetz M, Stevens CJ, Williams RJ, Fierer N (2015) Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18: 85–95.Google Scholar
- Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zaj B (ed) Biology of Anaerobic Microorganisms. John Wiley and Sons, New York, pp 179–244Google Scholar
- Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5: 1067–1071Google Scholar
- Voigt C, Marushchak ME, Lamprecht RE, Jackowicz-Korczyński M, Lindgren A, Mastepanov M, Granlund L, Christensen TR, Tahvanainen T, Martikainen PJ, Biasi C (2017a) Increased nitrous oxide emissions from Arctic peatlands after permafrost thaw. Proc Natl Acad Sci USA 114:6238–6243CrossRefGoogle Scholar
- Zhang JW, Wang JT, Chen W, Li B, Zhao K (1988) Vegetation of Xizang (Tibet). Science Press, BeijingGoogle Scholar
- Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol R 61:533–616Google Scholar