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      Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients

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          Abstract

          Terrestrial ecosystems are receiving elevated inputs of nitrogen (N) from anthropogenic sources and understanding how these increases in N availability affect soil microbial communities is critical for predicting the associated effects on belowground ecosystems. We used a suite of approaches to analyze the structure and functional characteristics of soil microbial communities from replicated plots in two long-term N fertilization experiments located in contrasting systems. Pyrosequencing-based analyses of 16S rRNA genes revealed no significant effects of N fertilization on bacterial diversity, but significant effects on community composition at both sites; copiotrophic taxa (including members of the Proteobacteria and Bacteroidetes phyla) typically increased in relative abundance in the high N plots, with oligotrophic taxa (mainly Acidobacteria) exhibiting the opposite pattern. Consistent with the phylogenetic shifts under N fertilization, shotgun metagenomic sequencing revealed increases in the relative abundances of genes associated with DNA/RNA replication, electron transport and protein metabolism, increases that could be resolved even with the shallow shotgun metagenomic sequencing conducted here (average of 75 000 reads per sample). We also observed shifts in the catabolic capabilities of the communities across the N gradients that were significantly correlated with the phylogenetic and metagenomic responses, indicating possible linkages between the structure and functioning of soil microbial communities. Overall, our results suggest that N fertilization may, directly or indirectly, induce a shift in the predominant microbial life-history strategies, favoring a more active, copiotrophic microbial community, a pattern that parallels the often observed replacement of K-selected with r-selected plant species with elevated N.

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          Most cited references 20

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          Functional metagenomic profiling of nine biomes.

          Microbial activities shape the biogeochemistry of the planet and macroorganism health. Determining the metabolic processes performed by microbes is important both for understanding and for manipulating ecosystems (for example, disruption of key processes that lead to disease, conservation of environmental services, and so on). Describing microbial function is hampered by the inability to culture most microbes and by high levels of genomic plasticity. Metagenomic approaches analyse microbial communities to determine the metabolic processes that are important for growth and survival in any given environment. Here we conduct a metagenomic comparison of almost 15 million sequences from 45 distinct microbiomes and, for the first time, 42 distinct viromes and show that there are strongly discriminatory metabolic profiles across environments. Most of the functional diversity was maintained in all of the communities, but the relative occurrence of metabolisms varied, and the differences between metagenomes predicted the biogeochemical conditions of each environment. The magnitude of the microbial metabolic capabilities encoded by the viromes was extensive, suggesting that they serve as a repository for storing and sharing genes among their microbial hosts and influence global evolutionary and metabolic processes.
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            Examining the global distribution of dominant archaeal populations in soil.

            Archaea, primarily Crenarchaeota, are common in soil; however, the structure of soil archaeal communities and the factors regulating their diversity and abundance remain poorly understood. Here, we used barcoded pyrosequencing to comprehensively survey archaeal and bacterial communities in 146 soils, representing a multitude of soil and ecosystem types from across the globe. Relative archaeal abundance, the percentage of all 16S rRNA gene sequences recovered that were archaeal, averaged 2% across all soils and ranged from 0% to >10% in individual soils. Soil C:N ratio was the only factor consistently correlated with archaeal relative abundances, being higher in soils with lower C:N ratios. Soil archaea communities were dominated by just two phylotypes from a constrained clade within the Crenarchaeota, which together accounted for >70% of all archaeal sequences obtained in the survey. As one of these phylotypes was closely related to a previously identified putative ammonia oxidizer, we sampled from two long-term nitrogen (N) addition experiments to determine if this taxon responds to experimental manipulations of N availability. Contrary to expectations, the abundance of this dominant taxon, as well as archaea overall, tended to decline with increasing N. This trend was coupled with a concurrent increase in known N-oxidizing bacteria, suggesting competitive interactions between these groups.
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              Toward an ecological classification of soil bacteria.

              Although researchers have begun cataloging the incredible diversity of bacteria found in soil, we are largely unable to interpret this information in an ecological context, including which groups of bacteria are most abundant in different soils and why. With this study, we examined how the abundances of major soil bacterial phyla correspond to the biotic and abiotic characteristics of the soil environment to determine if they can be divided into ecologically meaningful categories. To do this, we collected 71 unique soil samples from a wide range of ecosystems across North America and looked for relationships between soil properties and the relative abundances of six dominant bacterial phyla (Acidobacteria, Bacteroidetes, Firmicutes, Actinobacteria, alpha-Proteobacteria, and the beta-Proteobacteria). Of the soil properties measured, net carbon (C) mineralization rate (an index of C availability) was the best predictor of phylum-level abundances. There was a negative correlation between Acidobacteria abundance and C mineralization rates (r2 = 0.26, P < 0.001), while the abundances of beta-Proteobacteria and Bacteroidetes were positively correlated with C mineralization rates (r2 = 0.35, P < 0.001 and r2 = 0.34, P < 0.001, respectively). These patterns were explored further using both experimental and meta-analytical approaches. We amended soil cores from a specific site with varying levels of sucrose over a 12-month period to maintain a gradient of elevated C availabilities. This experiment confirmed our survey results: there was a negative relationship between C amendment level and the abundance of Acidobacteria (r2 = 0.42, P < 0.01) and a positive relationship for both Bacteroidetes and beta-Proteobacteria (r2 = 0.38 and 0.70, respectively; P < 0.01 for each). Further support for a relationship between the relative abundances of these bacterial phyla and C availability was garnered from an analysis of published bacterial clone libraries from bulk and rhizosphere soils. Together our survey, experimental, and meta-analytical results suggest that certain bacterial phyla can be differentiated into copiotrophic and oligotrophic categories that correspond to the r- and K-selected categories used to describe the ecological attributes of plants and animals. By applying the copiotroph-oligotroph concept to soil microorganisms we can make specific predictions about the ecological attributes of various bacterial taxa and better understand the structure and function of soil bacterial communities.
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                Author and article information

                Journal
                ISME J
                ISME J
                The ISME Journal
                Nature Publishing Group
                1751-7362
                1751-7370
                May 2012
                01 December 2011
                1 May 2012
                : 6
                : 5
                : 1007-1017
                Affiliations
                [1 ]Cooperative Institute for Research in Environmental Sciences, University of Colorado , Boulder, CO, USA
                [2 ]Department of Ecology and Evolutionary Biology, University of Colorado , Boulder, CO, USA
                [3 ]Department of Molecular, Cellular, and Developmental Biology, University of Colorado , Boulder, CO, USA
                [4 ]School of Forestry and Environmental Studies, Yale University , New Haven, CT, USA
                [5 ]Department of Chemistry and Biochemistry, University of Colorado , Boulder, CO, USA
                [6 ]Howard Hughes Medical Institute , Chevy Chase, MD, USA
                Author notes
                [* ]Cooperative Institute for Research in Environmental Sciences, University of Colorado at Boulder , Campus Box 216 UCB, Boulder, CO 80309-0216, USA. E-mail: Noah.Fierer@ 123456colorado.edu
                Article
                ismej2011159
                10.1038/ismej.2011.159
                3329107
                22134642
                Copyright © 2012 International Society for Microbial Ecology

                This work is licensed under the Creative Commons Attribution-NonCommercial-No Derivative Works 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/

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