Abstract
Above- and below-ground organisms are closely linked, but how elevational distribution pattern of soil microbes shifting across the treeline still remains unknown. Sampling of 140 plots with transect, we herein investigated soil bacterial distribution pattern from a temperate forest up to a subalpine meadow along an elevational gradient using Illumina sequencing. Our results revealed distinct elevational patterns of bacterial diversity above and below the treeline in responding to changes in soil conditions: a hollow elevational pattern in the forest (correlated with soil temperature, pH, and C:N ratio) and a significantly decreasing pattern in the meadow (correlated with soil pH, and available phosphorus). The bacterial community structure was also distinct between the forest and meadow, relating to soil pH in the forest and soil temperature in the meadow. Soil bacteria did not follow the distribution pattern of herb diversity, but bacterial community structure could be predicted by herb community composition. These results suggest that plant communities have an important influence on soil characteristics, and thus change the elevational distribution of soil bacteria. Our findings are useful for future assessments of climate change impacts on microbial community.
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References
Akaike, H. (1987). Factor analysis and AIC. Psychometrika 52, 317–332.
Bachman, S., Baker, W.J., Brummitt, N., Dransfield, J., and Moat, J. (2004). Elevational gradients, area and tropical island diversity: an example from the palms of New Guinea. Ecography 27, 299–310.
Bahram, M., Polme, S., Kõljalg, U., Zarre, S., and Tedersoo, L. (2012). Regional and local patterns of ectomycorrhizal fungal diversity and community structure along an altitudinal gradient in the Hyrcanian forests of northern Iran. New Phytol 193, 465–473.
Baker, K.L., Langenheder, S., Nicol, G.W., Ricketts, D., Killham, K., Campbell, C.D., and Prosser, J.I. (2009). Environmental and spatial characterisation of bacterial community composition in soil to inform sampling strategies. Soil Biol Biochem 41, 2292–2298.
Biddle, J.F., Fitz-Gibbon, S., Schuster, S.C., Brenchley, J.E., and House, C.H. (2008). Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment. Proc Natl Acad Sci USA 105, 10583–10588.
Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.
Bryant, J.A., Lamanna, C., Morlon, H., Kerkhoff, A.J., Enquist, B.J., and Green, J.L. (2008). Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci USA 105, 11505–11511.
Caporaso, J.G., Bittinger, K., Bushman, F.D., DeSantis, T.Z., Andersen, G.L., and Knight, R. (2010a). PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26, 266–267.
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., and Gordon, J.I. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335–336.
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N., Owens, S.M., Betley, J., Fraser, L., and Bauer, M. (2012). Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6, 1621–1624.
Cline, L.C., and Zak, D.R. (2015). Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96, 3374–3385.
Cornfield, A. (1960). Ammonia released on treating soils with N sodium hydroxide as a possible means of predicting the nitrogen-supplying power of soils. Nature 187, 260–261.
De Deyn, G.B., and Van der Putten, W.H. (2005). Linking aboveground and belowground diversity. Trends Ecol Evol 20, 625–633.
Dequiedt, S., Thioulouse, J., Jolivet, C., Saby, N.P., Lelievre, M., Maron, P.A., Martin, M.P., Prevost-Boure, N.C., Toutain, B., Arrouays, D., Lemanceau, P., and Ranjard, L. (2009). Biogeographical patterns of soil bacterial communities. Environ Microbiol Rep 1, 251–255.
Ding, J., Zhang, Y., Deng, Y., Cong, J., Lu, H., Sun, X., Yang, C., Yuan, T., Van Nostrand, J.D., and Li, D. (2015). Integrated metagenomics and network analysis of soil microbial community of the forest timberline. Sci Rep 5, 7994.
Diniz-Filho, J.A.F., and Bini, L.M. (2005). Modelling geographical patterns in species richness using eigenvector-based spatial filters. Global Ecol Biogeogr 14, 177–185.
Edgar, R.C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461.
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.
Faith, D.P. (1992). Conservation evaluation and phylogenetic diversity. Biol Conserv 61, 1–10.
Fierer, N., and Jackson, R.B. (2006). The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103, 626–631.
Fierer, N., McCain, C.M., Meir, P., Zimmermann, M., Rapp, J.M., Silman, M.R., and Knight, R. (2011). Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92, 797–804.
Finlay, B.J. (2002). Global dispersal of free-living microbial eukaryote species. Science 296, 1061–1063.
Goslee, S.C., and Urban, D.L. (2007). The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22, 1–19.
Griffiths, R.I., Thomson, B.C., James, P., Bell, T., Bailey, M., and Whiteley, A.S. (2011). The bacterial biogeography of British soils. Environ Microbiol 13, 1642–1654.
Guo, Q., Kelt, D.A., Sun, Z., Liu, H., Hu, L., Ren, H., and Wen, J. (2013). Global variation in elevational diversity patterns. Sci Rep 3, 3007–3007.
Harrell, F.E. (2001). Regression Modeling Strategies, with Applications to Linear Models, Survival Analysis and Logistic Regression (New York: Springer Press).
Harsch, M.A., Hulme, P.E., McGlone, M.S., and Duncan, R.P. (2009). Are treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol Lett 12, 1040–1049.
Hooper, D.U., Bignell, D.E., Brown, V.K., Brussard, L., Mark Dangerfield, J., Wall, D.H., Wardle, D.A., Coleman, D.C., Giller, K.E., and Lavelle, P. (2000). Interactions between aboveground and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. Bioscience 50, 1049–1061.
Jiang, XP,and Hu, XH. (2014). Inferring microbial interaction networks based on consensus similarity network fusion. Sci China Life Sci 57, 1115–1120.
Körner, C. (1998). A re-assessment of high elevation treeline positions and their explanation. Oecologia 115, 445–459.
Körner, C. (2007). The use of “altitude” in ecological research. Trends Ecol Evol 22, 569–574.
Landesman, W.J., Nelson, D.M., and Fitzpatrick, M.C. (2014). Soil properties and tree species drive diversity of soil bacterial communities. Soil Biol Biochem 76, 201–209.
Lauber, C.L., Hamady, M., Knight, R., and Fierer, N. (2009). Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75, 5111–5120.
Lichstein, J.W. (2007). Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecol 188, 117–131.
Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., Liu, X., and Wang, G. (2014). High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biol Biochem 70, 113–122.
Logares, R., Sunagawa, S., Salazar, G., Cornejo-Castillo, F.M., Ferrera, I., Sarmento, H., Hingamp, P., Ogata, H., Vargas, C., and Lima-Mendez, G. (2014). Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities. Environ Microbiol 16, 2659–2671.
Lomolino, M. (2001). Elevation gradients of species-density: historical and prospective views. Global Ecol Biogeogr 10, 3–13.
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J., Hector, A., Hooper, D., Huston, M., Raffaelli, D., and Schmid, B. (2001). Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808.
Magoc, T., and Salzberg, S.L. (2011). FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963.
Martiny, J.B.H., Eisen, J.A., Penn, K., Allison, S.D., and Horner-Devine, M.C. (2011). Drivers of bacterial beta-diversity depend on spatial scale. Proc Natl Acad Sci USA 108, 7850–7854.
McCain, C.M. (2005). Elevational gradients in diversity of small mammals. Ecology 86, 366–372.
McDonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., Andersen, G.L., Knight, R., and Hugenholtz, P. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6, 610–618.
McNown, R.W., and Sullivan, P.F. (2013). Low photosynthesis of treeline white spruce is associated with limited soil nitrogen availability in the Western Brooks Range, Alaska. Funct Ecol 27, 672–683.
Millard, P., and Singh, B. (2010). Does grassland vegetation drive soil microbial diversity? Nutr Cycl Agroecosyst 88, 147–158.
Miyamoto, Y., Nakano, T., Hattori, M., and Nara, K. (2014). The mid-domain effect in ectomycorrhizal fungi: range overlap along an elevation gradient on Mount Fuji, Japan. ISME J 8, 1739–1746.
Nicol, G.W., Leininger, S., Schleper, C., and Prosser, J.I. (2008). The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10, 2966–2978.
Prober, S.M., Leff, J.W., Bates, S.T., Borer, E.T., Firn, J., Harpole, W.S., Lind, E.M., Seabloom, E.W., Adler, P.B., and Bakker, J.D. (2015). Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol Lett 18, 85–95.
Rahbek, C. (1995). The elevational gradient of species richness: a uniform pattern? Ecography 18, 200–205.
Rahbek, C. (2005). The role of spatial scale and the perception of large-scale species richness patterns. Ecol Lett 8, 224–239.
Rangel, T.F., Diniz-Filho, J.A.F., and Bini, L.M. (2010). SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33, 46–50.
R Development Core Team. (2013). R: A Language and Environment for Statistical Computing (Vienna: R Foundation for Statistical Computing).
Shen, C., Liang, W., Shi, Y., Lin, X., Zhang, H., Wu, X., Xie, G., Chain, P., Grogan, P., and Chu, H. (2014). Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95, 3190–3202.
Shen, C., Ni, Y., Liang, W., Wang, J., and Chu, H. (2015). Distinct soil bacterial communities along a small-scale elevational gradient in alpine tundra. Front Microbiol 6, 582.
Shen, C., Xiong, J., Zhang, H., Feng, Y., Lin, X., Li, X., Liang, W., and Chu, H. (2013). Soil pH drives the spatial distribution of bacterial communities along elevation on Changbai Mountain. Soil Biol Biochem 57, 204–211.
Singh, D., Lee-Cruz, L., Kim, W.S., Kerfahi, D., Chun, J.H., and Adams, J.M. (2014). Strong elevational trends in soil bacterial community composition on Mt. Halla, South Korea. Soil Biol Biochem 68, 140–149.
Singh, D., Takahashi, K., Kim, M., Chun, J., and Adams, J.M. (2012). A hump-backed trend in bacterial diversity with elevation on Mount Fuji, Japan. Microb Ecol 63, 429–437.
Stevens, G.C. (1992). The elevational gradient in altitudinal range: an extension of Rapoport’s latitudinal rule to altitude. Am Nat 140, 893–911.
Sun, D.L, Jiang, X., Wu, Q.L., and Zhou, N.Y. (2013). Intragenomic heterogeneity of 16S rRNA genes causes overestimation of prokaryotic diversity. Appl Environ Microbiol 79, 5962–5969.
Tedersoo, L., Bahram, M., Põ lme, S., Kõ ljalg, U., Yorou, N.S., Wijesundera, R., Ruiz, L.V., Vasco-Palacios, A.M., Thu, P.Q., and Suija, A. (2014). Global diversity and geography of soil fungi. Science 346, 1256688.
Thébault, A., Clément, J.C., Ibanez, S., Roy, J., Geremia, R.A., Pérez, C.A., Buttler, A., Estienne, Y., and Lavorel, S. (2014). Nitrogen limitation and microbial diversity at the treeline. Oikos 123, 729–740.
Urbanová, M., Šnajdr, J., and 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 Der Heijden, M.G., Bardgett, R.D., and Van Straalen, N.M. (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11, 296–310.
Walkley, A. (1947). A critical examination of a rapid method for determining organic carbon in soils-Effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63, 251–264.
Wang, J.T., Cao, P., Hu, H.W., Li, J., Han, L.L., Zhang, L.M., Zheng, Y.M., and He, J.Z. (2015a). Altitudinal distribution patterns of soil bacterial and archaeal communities along Mt. Shegyla on the Tibetan Plateau. Microb Ecol 69, 135–145.
Wang, J.T., Zheng, Y.M., Hu, H.W., Zhang, L.M., Li, J., and He, J.Z. (2015b). Soil pH determines the alpha diversity but not beta diversity of soil fungal community along altitude in a typical Tibetan forest ecosystem. J Soils Sediments 15, 1224–1232.
Wang, J.J, Soininen, J., He, J., and Shen, J. (2012a). Phylogenetic clustering increases with elevation for microbes. Environ Microbiol Rep 4, 217–226.
Wang, J.J, Soininen, J., Zhang, Y., Wang, B., Yang, X., and Shen, J. (2011). Contrasting patterns in elevational diversity between microorganisms and macroorganisms. J Biogeogr 38, 595–603.
Wang, J.J., Soininen, J., Zhang, Y., Wang, B.X., Yang, X.D., and Shen, J. (2012b). Patterns of elevational beta diversity in micro- and macroorganisms. Global Ecol Biogeogr 21, 743–750.
Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setälä, H., Van Der Putten, W.H., and Wall, D.H. (2004). Ecological linkages between aboveground and belowground biota. Science 304, 1629–1633.
Zhang, Y., Cong, J., Lu, H., Li, G., Xue, Y., Deng, Y., Li, H., Zhou, J., and Li, D. (2015). Soil bacterial diversity patterns and drivers along an elevational gradient on Shennongjia Mountain, China. Microb Biotechnol 8, 739–746.
Zobel, M., and Öpik, M. (2014). Plant and arbuscular mycorrhizal fungal (AMF) communities-which drives which? J Veg Sci 25, 1133–1140.
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Li, G., Xu, G., Shen, C. et al. Contrasting elevational diversity patterns for soil bacteria between two ecosystems divided by the treeline. Sci. China Life Sci. 59, 1177–1186 (2016). https://doi.org/10.1007/s11427-016-0072-6
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DOI: https://doi.org/10.1007/s11427-016-0072-6