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      Global Biogeographic Analysis of Methanogenic Archaea Identifies Community-Shaping Environmental Factors of Natural Environments

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          Abstract

          Methanogenic archaea are important for the global greenhouse gas budget since they produce methane under anoxic conditions in numerous natural environments such as oceans, estuaries, soils, and lakes. Whether and how environmental change will propagate into methanogenic assemblages of natural environments remains largely unknown owing to a poor understanding of global distribution patterns and environmental drivers of this specific group of microorganisms. In this study, we performed a meta-analysis targeting the biogeographic patterns and environmental controls of methanogenic communities using 94 public mcrA gene datasets. We show a global pattern of methanogenic archaea that is more associated with habitat filtering than with geographical dispersal. We identify salinity as the control on methanogenic community composition at global scale whereas pH and temperature are the major controls in non-saline soils and lakes. The importance of salinity for structuring methanogenic community composition is also reflected in the biogeography of methanogenic lineages and the physiological properties of methanogenic isolates. Linking methanogenic alpha-diversity with reported values of methane emission identifies estuaries as the most diverse methanogenic habitats with, however, minor contribution to the global methane budget. With salinity, temperature and pH our study identifies environmental drivers of methanogenic community composition facing drastic changes in many natural environments at the moment. However, consequences of this for the production of methane remain elusive owing to a lack of studies that combine methane production rate with community analysis.

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          Most cited references62

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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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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              Methanogenic archaea: ecologically relevant differences in energy conservation.

              Most methanogenic archaea can reduce CO(2) with H(2) to methane, and it is generally assumed that the reactions and mechanisms of energy conservation that are involved are largely the same in all methanogens. However, this does not take into account the fact that methanogens with cytochromes have considerably higher growth yields and threshold concentrations for H(2) than methanogens without cytochromes. These and other differences can be explained by the proposal outlined in this Review that in methanogens with cytochromes, the first and last steps in methanogenesis from CO(2) are coupled chemiosmotically, whereas in methanogens without cytochromes, these steps are energetically coupled by a cytoplasmic enzyme complex that mediates flavin-based electron bifurcation.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                18 July 2017
                2017
                : 8
                : 1339
                Affiliations
                [1] 1Section 5.3 Geomicrobiology, GFZ German Research Centre for Geosciences Potsdam, Germany
                [2] 2College of Electrical Engineering, Northwest University for Nationalities Lanzhou, China
                [3] 3State Key Laboratory of Frozen Soil Engineering, Northwest Institute of Eco-Environment and Resources, Chinese Academy of Sciences Lanzhou, China
                Author notes

                Edited by: Hongchen Jiang, Miami University, United States

                Reviewed by: Joseph Yavitt, Cornell University, United States; Wei Xie, Tongji University, China

                *Correspondence: Xi Wen, xiwen@ 123456gfz-potsdam.de Susanne Liebner, sliebner@ 123456gfz-potsdam.de

                This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2017.01339
                5513909
                28769904
                9e188292-d7d3-49d4-9bff-a7ca01590565
                Copyright © 2017 Wen, Yang, Horn, Winkel, Wagner and Liebner.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 14 May 2017
                : 03 July 2017
                Page count
                Figures: 7, Tables: 3, Equations: 0, References: 80, Pages: 13, Words: 0
                Funding
                Funded by: China Scholarship Council 10.13039/501100004543
                Award ID: 201408620031
                Funded by: Helmholtz-Gemeinschaft 10.13039/501100001656
                Award ID: Helmholtz Young Investigators Group of S.L. (VH-NG-919)
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                methanogenic archaea,mcra,biogeography,environmental drivers,salinity,ph,temperature

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