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      Microbes as Engines of Ecosystem Function: When Does Community Structure Enhance Predictions of Ecosystem Processes?

      research-article
      1 , 2 , 1 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 45 , 46 , 47 , 1 , 48
      Frontiers in Microbiology
      Frontiers Media S.A.
      microbial diversity, functional gene, statistical modeling, microbial ecology, ecosystem processes, respiration, nitrification, denitrification

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          Abstract

          Microorganisms are vital in mediating the earth’s biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: ‘When do we need to understand microbial community structure to accurately predict function?’ We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.

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          Most cited references43

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          Patterns and processes of microbial community assembly.

          Recent research has expanded our understanding of microbial community assembly. However, the field of community ecology is inaccessible to many microbial ecologists because of inconsistent and often confusing terminology as well as unnecessarily polarizing debates. Thus, we review recent literature on microbial community assembly, using the framework of Vellend (Q. Rev. Biol. 85:183-206, 2010) in an effort to synthesize and unify these contributions. We begin by discussing patterns in microbial biogeography and then describe four basic processes (diversification, dispersal, selection, and drift) that contribute to community assembly. We also discuss different combinations of these processes and where and when they may be most important for shaping microbial communities. The spatial and temporal scales of microbial community assembly are also discussed in relation to assembly processes. Throughout this review paper, we highlight differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly. We end by discussing the implications of microbial assembly processes for ecosystem function and biodiversity.
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            Soil biodiversity and soil community composition determine ecosystem multifunctionality.

            Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth's biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.
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              Cross-biome metagenomic analyses of soil microbial communities and their functional attributes.

              For centuries ecologists have studied how the diversity and functional traits of plant and animal communities vary across biomes. In contrast, we have only just begun exploring similar questions for soil microbial communities despite soil microbes being the dominant engines of biogeochemical cycles and a major pool of living biomass in terrestrial ecosystems. We used metagenomic sequencing to compare the composition and functional attributes of 16 soil microbial communities collected from cold deserts, hot deserts, forests, grasslands, and tundra. Those communities found in plant-free cold desert soils typically had the lowest levels of functional diversity (diversity of protein-coding gene categories) and the lowest levels of phylogenetic and taxonomic diversity. Across all soils, functional beta diversity was strongly correlated with taxonomic and phylogenetic beta diversity; the desert microbial communities were clearly distinct from the nondesert communities regardless of the metric used. The desert communities had higher relative abundances of genes associated with osmoregulation and dormancy, but lower relative abundances of genes associated with nutrient cycling and the catabolism of plant-derived organic compounds. Antibiotic resistance genes were consistently threefold less abundant in the desert soils than in the nondesert soils, suggesting that abiotic conditions, not competitive interactions, are more important in shaping the desert microbial communities. As the most comprehensive survey of soil taxonomic, phylogenetic, and functional diversity to date, this study demonstrates that metagenomic approaches can be used to build a predictive understanding of how microbial diversity and function vary across terrestrial biomes.
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                Author and article information

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                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                24 February 2016
                2016
                : 7
                : 214
                Affiliations
                [1] 1Institute of Arctic and Alpine Research, University of Colorado Boulder, Boulder CO, USA
                [2] 2Biological Sciences Division, Pacific Northwest National Laboratory, Richland WA, USA
                [3] 3US Department of Energy, Joint Genome Institute, Walnut Creek CA, USA
                [4] 4Department of Forest Ecology, Federal Research and Training Centre for Forests, Bundesforschungs- und Ausbildungszentrum für Wald Vienna, Austria
                [5] 5Department of Soil Science, University of Saskatchewan, Saskatoon SK, Canada
                [6] 6Helmholtz Centre for Environmental Research – Centre for Environmental Biotechnology Leipzig, Germany
                [7] 7Department of Natural Resources and Environmental Sciences, University of Illinois at Urbana-Champaign, Urbana IL, USA
                [8] 8Life and Environmental Sciences and Sierra Nevada Research Institute, University of California – Merced, Merced CA, USA
                [9] 9School of Medicine, Flinders University, Adelaide SA, Australia
                [10] 10Institut National de la Recherche Agronomique – Agroecology Dijon, France
                [11] 11Institute of Biological and Environmental Sciences, University of Aberdeen Aberdeen, UK
                [12] 12Irstea, UR MALY, Centre de Lyon-Villeurbanne Villeurbanne, France
                [13] 13Department of Biogeography and Global Change, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas Madrid, Spain
                [14] 14Environment Centre Wales, Bangor University Gwynedd, UK
                [15] 15Department of Microbiology and Ecosystem Science, University of Vienna Vienna, Austria
                [16] 16Häme University of Applied Sciences Hämeenlinna, Finland
                [17] 17School of Freshwater Sciences, University of Wisconsin-Milwaukee, Milwaukee WI, USA
                [18] 18Department of Surface Waters, Eawag: Swiss Federal Institute of Aquatic Science and Technology Kastanienbaum, Switzerland
                [19] 19Centre for Carbon, Water and Food, The University of Sydney, Sydney NSW, Australia
                [20] 20Institute of Landscape Ecology, University of Münster Münster, Germany
                [21] 21Department of Environmental and Biological Sciences, University of Eastern Finland Kuopio, Finland
                [22] 22Natural Resources Institute Vantaa, Finland
                [23] 23Institute of Soil Science and Site Ecology, Technische University Dresden, Germany
                [24] 24Institute of Aquatic Ecology, Facultat de Ciències, University of Girona Girona, Spain
                [25] 25Institute for Sustainability Sciences – Agroscope Zurich, Switzerland
                [26] 26CSIRO Agriculture Flagship, Crace ACT, Australia
                [27] 27Department of Biology, University of Texas at Tyler, Tyler TX, USA
                [28] 28EDF R&D, National Hydraulics and Environmental Laboratory Chatou, France
                [29] 29Department of Microbiology and Ecosystem Science, University of Vienna Vienna, Austria
                [30] 30Division of Terrestrial Ecosystem Research, Department of Microbiology and Ecosystem Science, University of Vienna Vienna, Austria
                [31] 31Department of Ecosystem and Conservation Sciences, University of Montana, Missoula MT, USA
                [32] 32Centro de Investigación y Docencia Económicas – Consejo Superior de Investigaciones Científicas Valencia, Spain
                [33] 33Department of Biological Science, Virginia Institute of Marine Science, Gloucester Point VA, USA
                [34] 34AES School of Natural Resources Sciences, North Dakota State University, Fargo ND, USA
                [35] 35LEPABE - Laboratory for Process Engineering, Environmental, Biotechnology and Energy, Faculdade de Engenharia da Universidade do Porto Porto, Portugal
                [36] 36Southern California Coastal Water Research Project Authority, Costa Mesa CA, USA
                [37] 37UMR, Interactions Sol Plante Atmosphère, INRA Bordeaux Villenave d’Ornon, France
                [38] 38Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences Uppsala, Sweden
                [39] 39Department of Biological Sciences, Virginia Polytechnic Institute, State University, Blacksburg VA, USA
                [40] 40Centre Tecnològic Forestal de Catalunya Solsona, Spain
                [41] 41Centre de Recerca Ecològica i Aplicacions Forestals, Cerdanyola del Vallès Barcelona, Spain
                [42] 42School of Civil and Environmental Engineering, Yonsei University Seoul, South Korea
                [43] 43Department of Applied Biological Chemistry, The University of Tokyo Tokyo, Japan
                [44] 44Department of Biomedicine, Biotechnology and Public Health, University of Cadiz Puerto Real, Spain
                [45] 45Research Centre for Agrobiology and Pedology Florence, Italy
                [46] 46Department of Ecology and Genetics/Limnology, Uppsala University Uppsala, Sweden
                [47] 47Vale Living with Lakes Centre and Department of Biology, Laurentian University, Sudbury ON, Canada
                [48] 48Biology Department, Duke University, Durham NC, USA
                Author notes

                Edited by: Gary M. King, Louisiana State University, USA

                Reviewed by: Steffen Kolb, Landscape Biogeochemistry – Leibniz Centre for Agricultural Landscape Research, Germany; Hongchen Jiang, Miami University, USA; Kristen M. DeAngelis, University of Massachusetts Amherst, USA

                *Correspondence: Emily B. Graham, emily.graham@ 123456colorado.edu

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

                Article
                10.3389/fmicb.2016.00214
                4764795
                26941732
                995727d1-525c-40c8-8fbb-bc9943d1b3e4
                Copyright © 2016 Graham, Knelman, Schindlbacher, Siciliano, Breulmann, Yannarell, Beman, Abell, Philippot, Prosser, Foulquier, Yuste, Glanville, Jones, Angel, Salminen, Newton, Bürgmann, Ingram, Hamer, Siljanen, Peltoniemi, Potthast, Bañeras, Hartmann, Banerjee, Yu, Nogaro, Richter, Koranda, Castle, Goberna, Song, Chatterjee, Nunes, Lopes, Cao, Kaisermann, Hallin, Strickland, Garcia-Pausas, Barba, Kang, Isobe, Papaspyrou, Pastorelli, Lagomarsino, Lindström, Basiliko and Nemergut.

                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
                : 09 December 2015
                : 09 February 2016
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 68, Pages: 10, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: DEB-1221215
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                microbial diversity,functional gene,statistical modeling,microbial ecology,ecosystem processes,respiration,nitrification,denitrification

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