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      Temporal dynamics of hot desert microbial communities reveal structural and functional responses to water input

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          Abstract

          The temporal dynamics of desert soil microbial communities are poorly understood. Given the implications for ecosystem functioning under a global change scenario, a better understanding of desert microbial community stability is crucial. Here, we sampled soils in the central Namib Desert on sixteen different occasions over a one-year period. Using Illumina-based amplicon sequencing of the 16S rRNA gene, we found that α-diversity (richness) was more variable at a given sampling date (spatial variability) than over the course of one year (temporal variability). Community composition remained essentially unchanged across the first 10 months, indicating that spatial sampling might be more important than temporal sampling when assessing β-diversity patterns in desert soils. However, a major shift in microbial community composition was found following a single precipitation event. This shift in composition was associated with a rapid increase in CO 2 respiration and productivity, supporting the view that desert soil microbial communities respond rapidly to re-wetting and that this response may be the result of both taxon-specific selection and changes in the availability or accessibility of organic substrates. Recovery to quasi pre-disturbance community composition was achieved within one month after rainfall.

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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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            Responses of soil microbial communities to water stress: results from a meta-analysis.

            Soil heterotrophic respiration and nutrient mineralization are strongly affected by environmental conditions, in particular by moisture fluctuations triggered by rainfall events. When soil moisture decreases, so does decomposers' activity, with microfauna generally undergoing stress sooner than bacteria and fungi. Despite differences in the responses of individual decomposer groups to moisture availability (e.g., bacteria are typically more sensitive than fungi to water stress), we show that responses of decomposers at the community level are different in soils and surface litter, but similar across biomes and climates. This results in a nearly constant soil-moisture threshold corresponding to the point when biological activity ceases, at a water potential of about -14 MPa in mineral soils and -36 MPa in surface litter. This threshold is shown to be comparable to the soil moisture value where solute diffusion becomes strongly inhibited in soil, while in litter it is dehydration rather than diffusion that likely limits biological activity around the stress point. Because of these intrinsic constraints and lack of adaptation to different hydro-climatic regimes, changes in rainfall patterns (primary drivers of the soil moisture balance) may have dramatic impacts on soil carbon and nutrient cycling.
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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
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                29 September 2016
                2016
                : 6
                : 34434
                Affiliations
                [1 ]Centre for Microbial Ecology and Genomics (CMEG), Genomics Research Institute, Department of Genetics, University of Pretoria , Pretoria 0002, South Africa
                [2 ]Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory , Richland, WA 99352, USA
                [3 ]The Royal Agricultural University, Cirencester , Gloucestershire GL7 6JS, UK
                [4 ]School of Life Sciences, Heriot-Watt University , Edinburgh, EH14 4AS, UK
                [5 ]Gobabeb Training and Research Centre (GTRC) , Walvis Bay, Namibia
                [6 ]Animal, Plant and Environmental Sciences, University of Witwatersrand , Johannesburg, South Africa
                [7 ]Institute for Microbial Biotechnology and Metagenomics (IMBM). University of the Western Cape , Bellville 7535, South Africa
                Author notes
                Article
                srep34434
                10.1038/srep34434
                5041089
                27680878
                afa299a3-024d-4bc3-a1bc-62465109a9fe
                Copyright © 2016, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 21 June 2016
                : 14 September 2016
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