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      Distinct Biogeographic Patterns for Archaea, Bacteria, and Fungi along the Vegetation Gradient at the Continental Scale in Eastern China

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          Abstract

          Understanding biogeographic patterns is a precursor to improving our knowledge of the function of microbiomes and to predicting ecosystem responses to environmental change. Using natural forest soil samples from 110 locations, this study is one of the largest attempts to comprehensively understand the different patterns of soil archaeal, bacterial, and fungal biogeography at the continental scale in eastern China. These patterns in natural forest sites could ascertain reliable soil microbial biogeographic patterns by eliminating anthropogenic influences. This information provides guidelines for monitoring the belowground ecosystem’s decline and restoration. Meanwhile, the deviations in the soil microbial communities from corresponding natural forest states indicate the extent of degradation of the soil ecosystem. Moreover, given the association between vegetation type and the microbial community, this information could be used to predict the long-term response of the underground ecosystem to the vegetation distribution caused by global climate change.

          ABSTRACT

          The natural forest ecosystem in Eastern China, from tropical forest to boreal forest, has declined due to cropland development during the last 300 years, yet little is known about the historical biogeographic patterns and driving processes for the major domains of microorganisms along this continental-scale natural vegetation gradient. We predicted the biogeographic patterns of soil archaeal, bacterial, and fungal communities across 110 natural forest sites along a transect across four vegetation zones in Eastern China. The distance decay relationships demonstrated the distinct biogeographic patterns of archaeal, bacterial, and fungal communities. While historical processes mainly influenced bacterial community variations, spatially autocorrelated environmental variables mainly influenced the fungal community. Archaea did not display a distance decay pattern along the vegetation gradient. Bacterial community diversity and structure were correlated with the ratio of acid oxalate-soluble Fe to free Fe oxides (Feo/Fed ratio). Fungal community diversity and structure were influenced by dissolved organic carbon (DOC) and free aluminum (Ald), respectively. The role of these environmental variables was confirmed by the correlations between dominant operational taxonomic units (OTUs) and edaphic variables. However, most of the dominant OTUs were not correlated with the major driving variables for the entire communities. These results demonstrate that soil archaea, bacteria, and fungi have different biogeographic patterns and driving processes along this continental-scale natural vegetation gradient, implying different community assembly mechanisms and ecological functions for archaea, bacteria, and fungi in soil ecosystems.

          IMPORTANCE Understanding biogeographic patterns is a precursor to improving our knowledge of the function of microbiomes and to predicting ecosystem responses to environmental change. Using natural forest soil samples from 110 locations, this study is one of the largest attempts to comprehensively understand the different patterns of soil archaeal, bacterial, and fungal biogeography at the continental scale in eastern China. These patterns in natural forest sites could ascertain reliable soil microbial biogeographic patterns by eliminating anthropogenic influences. This information provides guidelines for monitoring the belowground ecosystem’s decline and restoration. Meanwhile, the deviations in the soil microbial communities from corresponding natural forest states indicate the extent of degradation of the soil ecosystem. Moreover, given the association between vegetation type and the microbial community, this information could be used to predict the long-term response of the underground ecosystem to the vegetation distribution caused by global climate change.

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          Most cited references41

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          The diversity and biogeography of soil bacterial communities.

          For centuries, biologists have studied patterns of plant and animal diversity at continental scales. Until recently, similar studies were impossible for microorganisms, arguably the most diverse and abundant group of organisms on Earth. Here, we present a continental-scale description of soil bacterial communities and the environmental factors influencing their biodiversity. We collected 98 soil samples from across North and South America and used a ribosomal DNA-fingerprinting method to compare bacterial community composition and diversity quantitatively across sites. Bacterial diversity was unrelated to site temperature, latitude, and other variables that typically predict plant and animal diversity, and community composition was largely independent of geographic distance. The diversity and richness of soil bacterial communities differed by ecosystem type, and these differences could largely be explained by soil pH (r(2) = 0.70 and r(2) = 0.58, respectively; P < 0.0001 in both cases). Bacterial diversity was highest in neutral soils and lower in acidic soils, with soils from the Peruvian Amazon the most acidic and least diverse in our study. Our results suggest that microbial biogeography is controlled primarily by edaphic variables and differs fundamentally from the biogeography of "macro" organisms.
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            Microbial biogeography: putting microorganisms on the map.

            We review the biogeography of microorganisms in light of the biogeography of macroorganisms. A large body of research supports the idea that free-living microbial taxa exhibit biogeographic patterns. Current evidence confirms that, as proposed by the Baas-Becking hypothesis, 'the environment selects' and is, in part, responsible for spatial variation in microbial diversity. However, recent studies also dispute the idea that 'everything is everywhere'. We also consider how the processes that generate and maintain biogeographic patterns in macroorganisms could operate in the microbial world.
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              Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                7 February 2017
                Jan-Feb 2017
                : 2
                : 1
                : e00174-16
                Affiliations
                [a ]Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, China
                [b ]Zhejiang Provincial Key Laboratory of Agricultural Resources and Environment, Hangzhou, China
                [c ]Department of Ecology and Evolution and Department of Surgery, University of Chicago, Chicago, Illinois, USA
                [d ]Department of Land, Air and Water Resources, University of California, Davis, Davis, California, USA
                [e ]Bioscience Division, Argonne National Laboratory, Lemont, Illinois, USA
                [f ]The Marine Biological Laboratory, Woods Hole, Massachusetts, USA
                University of Tennessee
                Author notes
                Address correspondence to Jianming Xu, jmxu@ 123456zju.edu.cn .

                Citation Ma B, Dai Z, Wang H, Dsouza M, Liu X, He Y, Wu J, Rodrigues JLM, Gilbert JA, Brookes PC, Xu J. 2017. Distinct biogeographic patterns for archaea, bacteria, and fungi along the vegetation gradient at the continental scale in Eastern China. mSystems 2:e00174-16. https://doi.org/10.1128/mSystems.00174-16.

                Author information
                http://orcid.org/0000-0002-6446-6462
                Article
                mSystems00174-16
                10.1128/mSystems.00174-16
                5296412
                28191504
                778f1116-584e-4bae-9770-2f00876db51b
                Copyright © 2017 Ma et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 19 November 2016
                : 5 January 2017
                Page count
                supplementary-material: 9, Figures: 7, Tables: 1, Equations: 0, References: 57, Pages: 14, Words: 9071
                Funding
                Funded by: Fundamental Research Funds for the Central Universities
                Award Recipient : Jianming Xu
                Funded by: The 111 Project
                Award ID: B060414
                Award Recipient : Jianming Xu
                Funded by: National Natural Science Foundation of China (NSFC) https://doi.org/10.13039/501100001809
                Award ID: 41520104001
                Award ID: 41130532
                Award Recipient : Jianming Xu
                Categories
                Research Article
                Ecological and Evolutionary Science
                Custom metadata
                January/February 2017

                eastern china,edaphic factors,forest soil,historical processes,microbial diversity,vegetation zone

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