Elevated carbon dioxide accelerates the spatial turnover of soil microbial communities

Although elevated CO2 (eCO2) significantly affects the α‐diversity, composition, function, interaction and dynamics of soil microbial communities at the local scale, little is known about eCO2 impacts on the geographic distribution of micro‐organisms regionally or globally. Here, we examined the β‐diversity of 110 soil microbial communities across six free air CO2 enrichment (FACE) experimental sites using a high‐throughput functional gene array. The β‐diversity of soil microbial communities was significantly (P < 0.05) correlated with geographic distance under both CO2 conditions, but declined significantly (P < 0.05) faster at eCO2 with a slope of −0.0250 than at ambient CO2 (aCO2) with a slope of −0.0231 although it varied within each individual site, indicating that the spatial turnover rate of soil microbial communities was accelerated under eCO2 at a larger geographic scale (e.g. regionally). Both distance and soil properties significantly (P < 0.05) contributed to the observed microbial β‐diversity. This study provides new hypotheses for further understanding their assembly mechanisms that may be especially important as global CO2 continues to increase.

[1]  D. W. Nelson,et al.  Total Carbon, Organic Carbon, and Organic Matter , 1983, SSSA Book Series.

[2]  Jizhong Zhou,et al.  Over 150 Years of Long-Term Fertilization Alters Spatial Scaling of Microbial Biodiversity , 2015, mBio.

[3]  Jizhong Zhou,et al.  Elevated CO2 shifts the functional structure and metabolic potentials of soil microbial communities in a C4 agroecosystem , 2015, Scientific Reports.

[4]  W. Admiraal,et al.  Eutrophication decreases distance decay of similarity in diatom communities , 2014 .

[5]  Yiqi Luo,et al.  Faster Decomposition Under Increased Atmospheric CO2 Limits Soil Carbon Storage , 2014, Science.

[6]  K. Peay,et al.  Endemism and functional convergence across the North American soil mycobiome , 2014, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Jizhong Zhou,et al.  Phylogenetic and functional gene structure shifts of the oral microbiomes in periodontitis patients , 2014, The ISME Journal.

[8]  Jizhong Zhou,et al.  Distinct responses of soil microbial communities to elevated CO2 and O3 in a soybean agro-ecosystem , 2013, The ISME Journal.

[9]  A. Arkin,et al.  Stochasticity, succession, and environmental perturbations in a fluidic ecosystem , 2014, Proceedings of the National Academy of Sciences.

[10]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[11]  P. Reich,et al.  Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass , 2013 .

[12]  J. Thioulouse,et al.  Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity , 2013, Nature Communications.

[13]  S. Bertilsson,et al.  Biogeography of bacterial communities exposed to progressive long-term environmental change , 2012, The ISME Journal.

[14]  B. Bohannan,et al.  Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities , 2012, Proceedings of the National Academy of Sciences.

[15]  Omri M. Finkel,et al.  Distance-Decay Relationships Partially Determine Diversity Patterns of Phyllosphere Bacteria on Tamarix Trees across the Sonoran Desert , 2012, Applied and Environmental Microbiology.

[16]  Susan M. Huse,et al.  Distance-Decay Relationships Partially Determine Diversity Patterns of Phyllosphere Bacteria on Tamrix Trees across the Sonoran Desert , 2012, Applied and Environmental Microbiology.

[17]  Jizhong Zhou,et al.  Applications of functional gene microarrays for profiling microbial communities. , 2012, Current opinion in biotechnology.

[18]  J. Fuhrman,et al.  Beyond biogeographic patterns: processes shaping the microbial landscape , 2012, Nature Reviews Microbiology.

[19]  R. B. Jackson,et al.  Common bacterial responses in six ecosystems exposed to 10 years of elevated atmospheric carbon dioxide. , 2012, Environmental microbiology.

[20]  B. Roe,et al.  Elevated Carbon Dioxide Alters the Structure of Soil Microbial Communities , 2012, Applied and Environmental Microbiology.

[21]  Jizhong Zhou,et al.  The phylogenetic composition and structure of soil microbial communities shifts in response to elevated carbon dioxide , 2011, The ISME Journal.

[22]  R. B. Jackson,et al.  Responses of soil cellulolytic fungal communities to elevated atmospheric CO₂ are complex and variable across five ecosystems. , 2011, Environmental microbiology.

[23]  R. B. Jackson,et al.  Atmospheric CO2 and soil extracellular enzyme activity: a meta‐analysis and CO2 gradient experiment , 2011 .

[24]  Jizhong Zhou,et al.  Phylogenetic Molecular Ecological Network of Soil Microbial Communities in Response to Elevated CO2 , 2011, mBio.

[25]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[26]  S. Allison,et al.  Drivers of bacterial β-diversity depend on spatial scale , 2011, Proceedings of the National Academy of Sciences.

[27]  Fay,et al.  Atmospheric CO 2 and soil extracellular enzyme activity : a meta-analysis and CO 2 gradient experiment , 2011 .

[28]  James Rosindell,et al.  Unified neutral theory of biodiversity and biogeography , 2010, Scholarpedia.

[29]  T. Bell Experimental tests of the bacterial distance–decay relationship , 2010, The ISME Journal.

[30]  Y. Carrillo,et al.  Contrasting effects of elevated CO2 and warming on nitrogen cycling in a semiarid grassland. , 2010, The New phytologist.

[31]  Jizhong Zhou,et al.  Metagenomic analysis reveals a marked divergence in the structure of belowground microbial communities at elevated CO2. , 2010, Ecology letters.

[32]  Christopher L. Hemme,et al.  GeoChip 3.0 as a high-throughput tool for analyzing microbial community composition, structure and functional activity , 2010, The ISME Journal.

[33]  J. Vorholt,et al.  Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere , 2010, The ISME Journal.

[34]  S. Blagodatsky,et al.  Elevated atmospheric CO2 increases microbial growth rates in soil: results of three CO2 enrichment experiments , 2010 .

[35]  R. McMurtrie,et al.  CO2 enhancement of forest productivity constrained by limited nitrogen availability , 2009, Proceedings of the National Academy of Sciences.

[36]  M. Bradford,et al.  Global patterns in belowground communities. , 2009, Ecology letters.

[37]  P. Reich,et al.  Interactive Effects of Time, CO2, N, and Diversity on Total Belowground Carbon Allocation and Ecosystem Carbon Storage in a Grassland Community , 2009, Ecosystems.

[38]  J. Six,et al.  Assessing the effect of elevated carbon dioxide on soil carbon: a comparison of four meta‐analyses , 2009 .

[39]  A. Rogers,et al.  Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. , 2009, Journal of experimental botany.

[40]  Elevated atmospheric CO 2 increases microbial growth rates in soil : results of three CO 2 enrichment experiments , 2009 .

[41]  R. B. Jackson,et al.  Soil carbon sequestration in a pine forest after 9 years of atmospheric CO2 enrichment , 2008 .

[42]  Charles T. Garten,et al.  Spatial scaling of functional gene diversity across various microbial taxa , 2008, Proceedings of the National Academy of Sciences.

[43]  Zhili He,et al.  Empirical Evaluation of a New Method for Calculating Signal-to-Noise Ratio for Microarray Data Analysis , 2008, Applied and Environmental Microbiology.

[44]  Soil carbon sequestration in a pine forest after 9 years of atmospheric CO 2 enrichment , 2008 .

[45]  J. Rousk,et al.  Fungal and bacterial growth in soil with plant materials of different C/N ratios. , 2007, FEMS microbiology ecology.

[46]  Sarah C. Goslee,et al.  The ecodist Package for Dissimilarity-based Analysis of Ecological Data , 2007 .

[47]  C. Cleveland,et al.  C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? , 2007 .

[48]  M. Korenberg,et al.  Microarray Data Analysis , 2007, Methods in Molecular Biology.

[49]  Bruce A. Hungate,et al.  Altered soil microbial community at elevated CO2 leads to loss of soil carbon , 2007, Proceedings of the National Academy of Sciences.

[50]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[51]  J. Hughes,et al.  A taxa–area relationship for bacteria , 2004, Nature.

[52]  Hans C. van Houwelingen,et al.  Microarray Data Analysis , 2004, Applied bioinformatics.

[53]  P. Dixon VEGAN, a package of R functions for community ecology , 2003 .

[54]  Campbell O. Webb,et al.  Phylogenies and Community Ecology , 2002 .

[55]  P. Reich,et al.  correction: Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition , 2001, Nature.

[56]  P. Reich,et al.  [Letters to nature] , 1975, Nature.

[57]  Marti J. Anderson,et al.  A new method for non-parametric multivariate analysis of variance in ecology , 2001 .

[58]  P. White,et al.  The distance decay of similarity in biogeography and ecology , 1999 .

[59]  José Costa,et al.  PicoGreen quantitation of DNA: effective evaluation of samples pre- or post-PCR , 1996, Nucleic Acids Res..

[60]  J. Tiedje,et al.  DNA recovery from soils of diverse composition , 1996, Applied and environmental microbiology.

[61]  P. Legendre,et al.  MODELING BRAIN EVOLUTION FROM BEHAVIOR: A PERMUTATIONAL REGRESSION APPROACH , 1994, Evolution; international journal of organic evolution.