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      Functional Gene Composition, Diversity and Redundancy in Microbial Stream Biofilm Communities

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          Abstract

          We surveyed the functional gene composition and diversity of microbial biofilm communities in 18 New Zealand streams affected by different types of catchment land use, using a comprehensive functional gene array, GeoChip 3.0. A total of 5,371 nutrient cycling and energy metabolism genes within 65 gene families were detected among all samples (342 to 2,666 genes per stream). Carbon cycling genes were most common, followed by nitrogen cycling genes, with smaller proportions of sulphur, phosphorus cycling and energy metabolism genes. Samples from urban and native forest streams had the most similar functional gene composition, while samples from exotic forest and rural streams exhibited the most variation. There were significant differences between nitrogen and sulphur cycling genes detected in native forest and urban samples compared to exotic forest and rural samples, attributed to contrasting proportions of nitrogen fixation, denitrification, and sulphur reduction genes. Most genes were detected only in one or a few samples, with only a small minority occurring in all samples. Nonetheless, 42 of 65 gene families occurred in every sample and overall proportions of gene families were similar among samples from contrasting streams. This suggests the existence of functional gene redundancy among different stream biofilm communities despite contrasting taxonomic composition.

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          Most cited references26

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          Stream biodiversity: the ghost of land use past.

          The influence of past land use on the present-day diversity of stream invertebrates and fish was investigated by comparing watersheds with different land-use history. Whole watershed land use in the 1950s was the best predictor of present-day diversity, whereas riparian land use and watershed land use in the 1990s were comparatively poor indicators. Our findings indicate that past land-use activity, particularly agriculture, may result in long-term modifications to and reductions in aquatic diversity, regardless of reforestation of riparian zones. Preservation of habitat fragments may not be sufficient to maintain natural diversity in streams, and maintenance of such biodiversity may require conservation of much or all of the watershed.
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            GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes.

            Owing to their vast diversity and as-yet uncultivated status, detection, characterization and quantification of microorganisms in natural settings are very challenging, and linking microbial diversity to ecosystem processes and functions is even more difficult. Microarray-based genomic technology for detecting functional genes and processes has a great promise of overcoming such obstacles. Here, a novel comprehensive microarray, termed GeoChip, has been developed, containing 24,243 oligonucleotide (50 mer) probes and covering >10,000 genes in >150 functional groups involved in nitrogen, carbon, sulfur and phosphorus cycling, metal reduction and resistance, and organic contaminant degradation. The developed GeoChip was successfully used for tracking the dynamics of metal-reducing bacteria and associated communities for an in situ bioremediation study. This is the first comprehensive microarray currently available for studying biogeochemical processes and functional activities of microbial communities important to human health, agriculture, energy, global climate change, ecosystem management, and environmental cleanup and restoration. It is particularly useful for providing direct linkages of microbial genes/populations to ecosystem processes and functions.
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              Riparian deforestation, stream narrowing, and loss of stream ecosystem services.

              A study of 16 streams in eastern North America shows that riparian deforestation causes channel narrowing, which reduces the total amount of stream habitat and ecosystem per unit channel length and compromises in-stream processing of pollutants. Wide forest reaches had more macroinvertebrates, total ecosystem processing of organic matter, and nitrogen uptake per unit channel length than contiguous narrow deforested reaches. Stream narrowing nullified any potential advantages of deforestation regarding abundance of fish, quality of dissolved organic matter, and pesticide degradation. These findings show that forested stream channels have a wider and more natural configuration, which significantly affects the total in-stream amount and activity of the ecosystem, including the processing of pollutants. The results reinforce both current policy of the United States that endorses riparian forest buffers as best management practice and federal and state programs that subsidize riparian reforestation for stream restoration and water quality. Not only do forest buffers prevent nonpoint source pollutants from entering small streams, they also enhance the in-stream processing of both nonpoint and point source pollutants, thereby reducing their impact on downstream rivers and estuaries.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 April 2015
                2015
                : 10
                : 4
                : e0123179
                Affiliations
                [1 ]School of Biological Sciences, University of Auckland, Auckland, New Zealand
                [2 ]Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK, United States of America
                Missouri University of Science and Technology, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GL GDL. Performed the experiments: AD GL ZH JZ. Analyzed the data: AD. Contributed reagents/materials/analysis tools: ZH JZ. Wrote the paper: AD GL GDL.

                Article
                PONE-D-14-39222
                10.1371/journal.pone.0123179
                4388685
                25849814
                c6b609d6-8c76-4d5d-bb7c-e6c7923bbfcf
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 3 September 2014
                : 17 February 2015
                Page count
                Figures: 5, Tables: 4, Pages: 21
                Funding
                This study was supported by the New Zealand Foundation for Research, Science and Technology UOAx306 (GDL) ( http://www.msi.govt.nz/) and the Royal Society of New Zealand Marsden Fund LIU0901 (GL) ( http://www.royalsociety.org.nz). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Research Article
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                All relevant data are within the paper and its Supporting Information files.

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