Community assemblage of free-living diazotrophs along the elevational gradient of Mount Gongga

Abstract

Mountain systems are unique for studying the responses of species distribution and diversity to environmental changes along elevational gradients. It is well known that free-living diazotrophic microorganisms are important to nitrogen cycling in mountain systems. However, the elevational patterns of free-living diazotrophs and the underlying ecological processes in controlling their turnover along broader gradients are less well documented. Here, we investigated the pattern of diazotrophic diversity along the elevational gradient (1800 m–4100 m) in Mount Gongga of China. The results showed that the α-diversity of diazotrophs did not change with the elevation from 1800 m to 2800 m, but decreased at elevations above 3000 m. Such diversity pattern was driven mainly by soil total carbon, nitrogen, and plant richness. Various diazotrophic taxa showed differential abundance-elevation relationships. Ecological processes determining diazotrophic community assemblage shift along the elevations. Deterministic processes were relatively stronger at both low and high elevations, whereas stochastic processes were stronger at the middle elevation. This study also suggested a strong relationship among aboveground plants and diazotrophs, highlighting their potential interactions, even for free-living diazotrophs.

Graphical abstract

Keywords

diazotrophs / community assemblage / elevational gradient / Mount Gongga

References

[1] Achberger, A.M., Michaud, A.B., Vick-Majors, T.J., Christner, B.C., Skidmore, M.L., Priscu, J.C., Tranter, M., 2017. Microbiology of subglacial environments, Psychrophiles: From Biodiversity to Biotechnology. Springer, pp. 83–110.

[2] Badri, D.V., Chaparro, J.M., Zhang, R., Shen, Q., Vivanco, J.M., 2013. Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry 288, 4502–4512

[3] Blaško, R., Bach, L.H., Yarwood, S.A., Trumbore, S.E., Högberg, P., Högberg, M.N., 2015. Shifts in soil microbial community structure, nitrogen cycling and the concomitant declining N availability in ageing primary boreal forest ecosystems. Soil Biology & Biochemistry 91, 200–211

[4] Broughton, W.J., Zhang, F., Perret, X., Staehelin, C., 2003. Signals exchanged between legumes and Rhizobium: agricultural uses and perspectives. Plant and Soil 252, 129–137

[5] Brown, J.H., 2001. Mammals on mountainsides: Elevational patterns of diversity. Global Ecology and Biogeography 10, 101–109

[6] Bryant, J.A., Lamanna, C., Morlon, H., Kerkhoff, A.J., Enquist, B.J., Green, J.L., 2008. Colloquium paper: microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proceedings of the National Academy of Sciences of the United States of America 105, 11505–11511

[7] Chao, A., 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics 11, 265–270.

[8] Chase, J.M., 2007a. Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences of the United States of America 104, 17430–17434

[9] Chase, J.M., 2007b. Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences of the United States of America 104, 17430–17434

[10] Chase, J.M., 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328, 1388–1391

[11] Chase, J.M., Myers, J.A., 2011. Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 366, 2351–2363

[12] Cheng, G., Luo, J., 2003. The carbon accumulation and dissipation features of sub-alpine woodland in Mt. Gongga. Journal of Geographical Sciences 13, 13–18

[13] Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in community structure. Austral Ecology 18, 117–143

[14] Collavino, M.M., Tripp, H.J., Frank, I.E., Vidoz, M.L., Calderoli, P.A., Donato, M., Zehr, J.P., Aguilar, O.M., 2014. nifH pyrosequencing reveals the potential for location-specific soil chemistry to influence N₂ -fixing community dynamics. Environmental Microbiology 16, 3211–3223

[15] DeLuca, T.H., Zackrisson, O., Nilsson, M.C., Sellstedt, A., 2002. Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419, 917–920

[16] Desgarennes, D., Garrido, E., Torres-Gomez, M.J., Peña-Cabriales, J.J., Partida-Martinez, L.P., 2014. Diazotrophic potential among bacterial communities associated with wild and cultivated Agave species. FEMS Microbiology Ecology 90, 844–857

[17] Dini-Andreote, F., Stegen, J.C., van Elsas, J.D., Salles, J.F., 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proceedings of the National Academy of Sciences of the United States of America 112, E1326–E1332

[18] Doane, T.A., Horwáth, W.R., 2003. Spectrophotometric determination of nitrate with a single reagent. Analytical Letters 36, 2713–2722

[19] Dumbrell, A.J., Nelson, M., Helgason, T., Dytham, C., Fitter, A.H., 2010. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME Journal 4, 337–345

[20] Elsen, P.R., Tingley, M.W., 2015. Global mountain topography and the fate of montane species under climate change. Nature Climate Change 5, 772–776

[21] Farnelid, H., Bentzon-Tilia, M., Andersson, A.F., Bertilsson, S., Jost, G., Labrenz, M., Jürgens, K., Riemann, L., 2013. Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME Journal 7, 1413–1423

[22] Fierer, N., McCain, C.M., Meir, P., Zimmermann, M., Rapp, J.M., Silman, M.R., Knight, R., 2011. Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92, 797–804

[23] Gower, J.C., 1966. Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53, 325–338

[24] Guo, H., Więski, K., Lan, Z., Pennings, S.C., 2014. Relative influence of deterministic processes on structuring marsh plant communities varies across an abiotic gradient. Oikos 123, 173–178.

[25] Harrison, S.P., Gornish, E.S., Copeland, S., 2015. Climate-driven diversity loss in a grassland community. Proceedings of the National Academy of Sciences of the United States of America 112, 8672–8677

[26] Hawkins, C.P., Mykrä, H., Oksanen, J., Vander Laan, J.J., 2015. Environmental disturbance can increase beta diversity of stream macroinvertebrate assemblages. Global Ecology and Biogeography 24, 483–494

[27] Hell, K., Edwards, A., Zarsky, J., Podmirseg, S.M., Girdwood, S., Pachebat, J.A., Insam, H., Sattler, B., 2013. The dynamic bacterial communities of a melting High Arctic glacier snowpack. ISME Journal 7, 1814–1826

[28] Huson, D.H., Auch, A.F., Qi, J., Schuster, S.C., 2007. MEGAN analysis of metagenomic data. Genome Research 17, 377–386

[29] Jump, A.S., Peñuelas, J., 2005. Running to stand still: Adaptation and the response of plants to rapid climate change. Ecology Letters 8, 1010–1020

[30] Lauber, C.L., Hamady, M., Knight, R., Fierer, N., 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and Environmental Microbiology 75, 5111–5120

[31] Leibold, M.A., McPeek, M.A., 2006. Coexistence of the niche and neutral perspectives in community ecology. Ecology 87, 1399–1410

[32] Li, J., Shen, Z., Li, C., Kou, Y., Wang, Y., Tu, B., Zhang, S., Li, X., 2018. Stair-step pattern of soil bacterial diversity mainly driven by pH and vegetation types along the elevational gradients of Gongga Mountain, China. Frontiers in Microbiology 9, 569

[33] Li, W., Yang, G., Chen, H., Tian, J., Zhang, Y., Zhu, Q.A., Peng, C., Yang, J.A., 2013. Soil available nitrogen, dissolved organic carbon and microbial biomass content along altitudinal gradient of the eastern slope of Gongga Mountain. Acta Ecologica Sinica 33, 266–271

[34] Liao, H., Li, Y., Yao, H., 2018. Fertilization with inorganic and organic nutrients changes diazotroph community composition and N-fixation rates. Journal of Soils and Sediments 18, 1076–1086

[35] Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., Liu, X., Wang, G., 2015. Soil carbon content drives the biogeographical distribution of fungal communities in the black soil zone of northeast China. Soil Biology & Biochemistry 83, 29–39

[36] Lu, X., Cheng, G., 2009. Climate change effects on soil carbon dynamics and greenhouse gas emissions in Abies fabri forest of subalpine, southwest China. Soil Biology & Biochemistry 41, 1015–1021

[37] McCain, C.M., 2005. Elevational gradients in diversity of small mammals. Ecology 86, 366–372

[38] Mooshammer, M., Wanek, W., Hämmerle, I., Fuchslueger, L., Hofhansl, F., Knoltsch, A., Schnecker, J., Takriti, M., Watzka, M., Wild, B., Keiblinger, K.M., Zechmeister-Boltenstern, S., Richter, A., 2014. Adjustment of microbial nitrogen use efficiency to carbon:nitrogen imbalances regulates soil nitrogen cycling. Nature Communications 5, 3694

[39] Myers, J.A., Chase, J.M., Jiménez, I., Jørgensen, P.M., Araujo-Murakami, A., Paniagua-Zambrana, N., Seidel, R., 2013. Beta-diversity in temperate and tropical forests reflects dissimilar mechanisms of community assembly. Ecology Letters 16, 151–157

[40] Nottingham, A.T., Fierer, N., Turner, B.L., Whitaker, J., Ostle, N.J., McNamara, N.P., Bardgett, R.D., Leff, J.W., Salinas, N., Silman, M.R., Kruuk, L.E.B., Meir, P., 2018. Microbes follow Humboldt: temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. bioRxiv 99, 2455–2466

[41] Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, M.H.H., Oksanen, M.J., Suggests, M., 2007. The vegan package. Community Ecology Package 10, 631–637.

[42] Pan, Y., Birdsey, R.A., Fang, J., Houghton, R., Kauppi, P.E., Kurz, W.A., Phillips, O.L., Shvidenko, A., Lewis, S.L., Canadell, J.G., Ciais, P., Jackson, R.B., Pacala, S.W., McGuire, A.D., Piao, S., Rautiainen, A., Sitch, S., Hayes, D., 2011. A large and persistent carbon sink in the world’s forests. Science 333, 988–993

[43] Paradis, E., Claude, J., Strimmer, K., 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics (Oxford, England) 20, 289–290

[44] Paul, E.A., 2016. The nature and dynamics of soil organic matter: Plant inputs, microbial transformations, and organic matter stabilization. Soil Biology & Biochemistry 98, 109–126

[45] Pettorelli, N., Gaillard, J.M., Mysterud, A., Duncan, P., Delorme, D., Van Laere, G., Toïgo, C., Klein, F., 2006. Using a proxy of plant productivity (NDVI) to find key periods for animal performance: The case of roe deer. Oikos 112, 565–572

[46] Piao, S., Nan, H., Huntingford, C., Ciais, P., Friedlingstein, P., Sitch, S., Peng, S., Ahlström, A., Canadell, J.G., Cong, N., Levis, S., Levy, P.E., Liu, L., Lomas, M.R., Mao, J., Myneni, R.B., Peylin, P., Poulter, B., Shi, X., Yin, G., Viovy, N., Wang, T., Wang, X., Zaehle, S., Zeng, N., Zeng, Z., Chen, A., 2014. Evidence for a weakening relationship between interannual temperature variability and northern vegetation activity. Nature Communications 5, 5018

[47] Poly, F., Monrozier, L.J., Bally, R., 2001. Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Research in Microbiology 152, 95–103

[48] Rahbek, C., 1995. The elevational gradient of species richness: A uniform pattern? Ecography 18, 200–205

[49] Rastetter, E.B., Vitousek, P.M., Field, C., Shaver, G.R., Herbert, D., Gren, G.I., 2001. Resource optimization and symbiotic nitrogen fixation. Ecosystems (New York, N.Y.) 4, 369–388

[50] Reed, S.C., Cleveland, C.C., Townsend, A.R., 2011. Functional ecology of free-living nitrogen fixation: A contemporary perspective. Annual Review of Ecology Evolution and Systematics 42, 489–512

[51] Reed, S.C., Cleveland, C.C., Townsend, A.R., 2013. Relationships among phosphorus, molybdenum and free-living nitrogen fixation in tropical rain forests: Results from observational and experimental analyses. Biogeochemistry 114, 135–147

[52] Rominger, A.J., Miller, T.E., Collins, S.L., 2009. Relative contributions of neutral and niche-based processes to the structure of a desert grassland grasshopper community. Oecologia 161, 791–800

[53] Rowe, R.J., Heaney, L.R., Rickart, E.A., 2015. Scale effects on the pattern and predictors of small mammal diversity along a local elevational gradient in the Great Basin. Journal of Biogeography 42, 1964–1974

[54] Rui, J., Li, J., Wang, S., An, J., Liu, W.T., Lin, Q., Yang, Y., He, Z., Li, X., 2015. Responses of bacterial communities to simulated climate changes in alpine meadow soil of the Qinghai-Tibet Plateau. Applied and Environmental Microbiology 81, 6070–6077

[55] Santos, H.F., Carmo, F.L., Duarte, G., Dini-Andreote, F., Castro, C.B., Rosado, A.S., van Elsas, J.D., Peixoto, R.S., 2014. Climate change affects key nitrogen-fixing bacterial populations on coral reefs. ISME Journal 8, 2272–2279

[56] Shannon, C.E., Weaver, W., Burks, A.W., 1951. The mathematical theory of communication 60, 3.

[57] Shen, C., Liang, W., Shi, Y., Lin, X., Zhang, H., Wu, X., Xie, G., Chain, P., Grogan, P., Chu, H., 2014. Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95, 3190–3202

[58] Shen, C., Xiong, J., Zhang, H., Feng, Y., Lin, X., Li, X., Liang, W., Chu, H., 2013. Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biology & Biochemistry 57, 204–211

[59] Shen, Z., Fang, J., Liu, Z., Wu, J., 2001. Patterns of biodiversity along the vertical vegetation spectrum of the east aspect of Gongga Mountain. Acta Phytoecologica Sinica 25, 721–732.

[60] Simpson, E.H., 1949. Measurement of diversity. Nature163–688.

[61] Singh, B.K., Bardgett, R.D., Smith, P., Reay, D.S., 2010. Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nature Reviews. Microbiology 8, 779–790

[62] Smith, M.A., Hallwachs, W., Janzen, D.H., 2014. Diversity and phylogenetic community structure of ants along a Costa Rican elevational gradient. Ecography 37, 720–731

[63] Sproull, G.J., Quigley, M.F., Sher, A., González, E., 2015. Long-term changes in composition, diversity and distribution patterns in four herbaceous plant communities along an elevational gradient. Journal of Vegetation Science 26, 552–563

[64] Sun, H., Wu, Y., Zhou, J., Bing, H., 2016. Variations of bacterial and fungal communities along a primary successional chronosequence in the Hailuogou glacier retreat area (Gongga Mountain, SW China). Journal of Mountain Science 13, 1621–1631

[65] Tang, Y., Zhang, M., Chen, A., Zhang, W., Wei, W., Sheng, R., 2017. Impact of fertilization regimes on diazotroph community compositions and N2-fixation activity in paddy soil. Agriculture, Ecosystems & Environment 247, 1–8

[66] Thébault, A., Clément, J.C., Ibanez, S., Roy, J., Geremia, R.A., Pérez, C.A., Buttler, A., Estienne, Y., Lavorel, S., 2014. Nitrogen limitation and microbial diversity at the treeline. Oikos 123, 729–740

[67] Tian, J., Wu, B., Chen, H., Jiang, N., Kang, X., Liu, X., 2017. Patterns and drivers of fungal diversity along an altitudinal gradient on Mount Gongga, China. Journal of Soils and Sediments 17, 1–10

[68] Tilman, D., 2004. Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proceedings of the National Academy of Sciences of the United States of America 101, 10854–10861

[69] van der Heijden, M.G., Bardgett, R.D., van Straalen, N.M., 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11, 296–310

[70] van der Heijden, M.G.A., Bakker, R., Verwaal, J., Scheublin, T.R., Rutten, M., van Logtestijn, R., Staehelin, C., 2006. Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiology Ecology 56, 178–187

[71] Vellend, M., Agrawal, A., 2010. Conceptual synthesis in community ecology. Quarterly Review of Biology 85, 183–206

[72] Vellend, M., Srivastava, D.S., Anderson, K.M., Brown, C.D., Jankowski, J.E., Kleynhans, E.J., Kraft, N.J., Letaw, A.D., Macdonald, A.A.M., Maclean, J.E., Myers-Smith, I.H., Norris, A.R., Xue, X., 2014. Assessing the relative importance of neutral stochasticity in ecological communities. Oikos 123, 1420–1430

[73] Vitousek, P.M., Howarth, R.W., 1991. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13, 87–115

[74] Wang, D., Xu, A., Elmerich, C., Ma, L.Z., 2017a. Biofilm formation enables free-living nitrogen-fixing rhizobacteria to fix nitrogen under aerobic conditions. ISME Journal 11, 1602–1613

[75] Wang, L., Ouyang, H., Zhou, C.P., Zhang, F., Song, M.H., Tian, Y.Q., 2005. Soil organic matter dynamics along a vertical vegetation gradient in the Gongga Mountain on the Tibetan Plateau. Journal of Integrative Plant Biology 47, 411–420

[76] Wang, Y., Li, C., Kou, Y., Wang, J., Tu, B., Li, H., Li, X., Wang, C., Yao, M., 2017b. Soil pH is a major driver of soil diazotrophic community assembly in Qinghai-Tibet alpine meadows. Soil Biology & Biochemistry 115, 547–555

[77] Wartiainen, I., Eriksson, T., Zheng, W., Rasmussen, U., 2008. Variation in the active diazotrophic community in rice paddy—nifH PCR-DGGE analysis of rhizosphere and bulk soil. Applied Soil Ecology 39, 65–75

[78] Weatherburn, M., 1967. Phenol-hypochlorite reaction for determination of ammonia. Analytical Chemistry 39, 971–974

[79] Wichard, T., Mishra, B., Myneni, S.C., Bellenger, J.P., Kraepiel, A.M., 2009. Storage and bioavailability of molybdenum in soils increased by organic matter complexation. Nature Geoscience 2, 625–629

[80] Wu, Y., Colwell, R.K., Rahbek, C., Zhang, C., Quan, Q., Wang, C., Lei, F., 2013a. Explaining the species richness of birds along a subtropical elevational gradient in the Hengduan Mountains. Journal of Biogeography 40, 2310–2323

[81] Wu, Y., Yang, Q., Wen, Z., Xia, L., Zhang, Q., Zhou, H., 2013b. What drives the species richness patterns of non-volant small mammals along a subtropical elevational gradient? Ecography 36, 185–196

[82] Zehr, J.P., Jenkins, B.D., Short, S.M., Steward, G.F., 2003. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environmental Microbiology 5, 539–554

[83] Zhang, X., Johnston, E.R., Liu, W., Li, L., Han, X., 2016. Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Global Change Biology 22, 198–207

[84] Zhou, J., Deng, Y., Zhang, P., Xue, K., Liang, Y., Van Nostrand, J.D., Yang, Y., He, Z., Wu, L., Stahl, D.A., Hazen, T.C., Tiedje, J.M., Arkin, A.P., 2014. Stochasticity, succession, and environmental perturbations in a fluidic ecosystem. Proceedings of the National Academy of Sciences of the United States of America 111, E836–E845

Acknowledgments

The work was supported by National Natural Science Foundation of China (41771293, 41630751, 31670503) and Chinese Academy of Sciences (XXH13503-03-106, XDB15010303), Open Fund of Key Laboratory of Environmental and Applied Microbiology CAS (KLCAS-2017-3, KLCAS-2016-03).

Electronic supplementary material

Supplementary material is available in the online version of this article at http://dx.doi.org/10.1007/s42832-019-013-y and is accessible for authorized users.

RIGHTS & PERMISSIONS

2019 Higher Education Press