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      Drivers of bacterial diversity dynamics in permeable carbonate and silicate coral reef sands from the Red Sea

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          Abstract

          Permeable sediments and associated microbial communities play a fundamental role in nutrient recycling within coral reef ecosystems by ensuring high levels of primary production in oligotrophic environments. A previous study on organic matter degradation within biogenic carbonate and terrigenous silicate reef sands in the Red Sea suggested that observed sand-specific differences in microbial activity could be caused by variations in microbial biomass and diversity. Here, we tested this hypothesis by comparing bacterial abundance and community structure in both sand types, and by further exploring the structuring effects of time (season) and space (sediment depth, in/out-reef). Changes in bacterial community structure, as determined via automated ribosomal intergenic spacer analysis (ARISA), were primarily driven by sand mineralogy at specific seasons, sediment depths and reef locations. By coupling ARISA with 16S-ITS rRNA sequencing, we detected significant community shifts already at the bacterial class level, with Proteobacteria ( Gamma-, Delta-, Alpha-) and Actinobacteria being prominent members of the highly diverse communities. Overall, our findings suggest that reef sand-associated bacterial communities vary substantially with sand type. Especially in synergy with environmental variation over time and space, mineralogical differences seem to play a central role in maintaining high levels of bacterial community heterogeneity. The local co-occurrence of carbonate and silicate sands may thus significantly increase the availability of microbial niches within a single coral reef ecosystem.

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          Most cited references51

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          rRNA operon copy number reflects ecological strategies of bacteria.

          Although natural selection appears to favor the elimination of gene redundancy in prokaryotes, multiple copies of each rRNA-encoding gene are common on bacterial chromosomes. Despite this conspicuous deviation from single-copy genes, no phenotype has been consistently associated with rRNA gene copy number. We found that the number of rRNA genes correlates with the rate at which phylogenetically diverse bacteria respond to resource availability. Soil bacteria that formed colonies rapidly upon exposure to a nutritionally complex medium contained an average of 5.5 copies of the small subunit rRNA gene, whereas bacteria that responded slowly contained an average of 1.4 copies. In soil microcosms pulsed with the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D), indigenous populations of 2,4-D-degrading bacteria with multiple rRNA genes ( = 5.4) became dominant, whereas populations with fewer rRNA genes ( = 2.7) were favored in unamended controls. These findings demonstrate phenotypic effects associated with rRNA gene copy number that are indicative of ecological strategies influencing the structure of natural microbial communities.
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            Multiscale responses of microbial life to spatial distance and environmental heterogeneity in a patchy ecosystem.

            Spatial distance (SD) and environmental heterogeneity (EH) are currently thought to represent major factors shaping genetic variation and population abundance, but their relative importance is still poorly understood. Because EH varies at multiple spatial scales, so too are microbial variables expected to vary. The determination of SD x EH interactions at multiple scales is, however, not a trivial exercise, especially when one examines their effects on microbial abundance and genomic similarities. Here we assessed those interactions at all scales perceptible in a patchy environment composed of known plant species and of heterogeneous soil physical and chemical parameters. For free-living, soil-borne Burkholderia ambifaria, genomic similarities responded to most of the spatial scales that the experimental sampling scheme could reveal, despite limited dispersal of the individuals. Species abundance and community composition were, however, responding to much smaller scales more consistent with local responses to EH. Our results suggest that whole-genome similarities may reflect the simultaneous effects of both SD and EH in microbial populations, but the pure effects of each factor only contributed to < 2% of the total genetic variation. The large amount of unexplained variation that remains after considering most environmental, spatial, and biological interactions is then posited to be the result of noise introduced by unmeasured environmental and spatial variability, sampling effects, and neutral ecological drift.
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              Comparison of different primer sets for use in automated ribosomal intergenic spacer analysis of complex bacterial communities.

              ITSF and ITSReub, constituting a new primer set designed for the amplification of the 16S-23S rRNA intergenic transcribed spacers, have been compared with primer sets consisting of 1406F and 23Sr (M. M. Fisher and E. W. Triplett, Appl. Environ. Microbiol. 65:4630-4636, 1999) and S-D-Bact-1522-b-S-20 and L-D-Bact-132-a-A-18 (L. Ranjard et al., Appl. Environ. Microbiol. 67:4479-4487, 2001), previously proposed for automated ribosomal intergenic spacer analysis (ARISA) of complex bacterial communities. An agricultural soil and a polluted soil, maize silage, goat milk, a small marble sample from the facade of the Certosa of Pavia (Pavia, Italy), and brine from a deep hypersaline anoxic basin in the Mediterranean Sea were analyzed with the three primer sets. The number of peaks in the ARISA profiles, the range of peak size (width of the profile), and the reproducibility of results were used as indices to evaluate the efficiency of the three primer sets. The overall data showed that ITSF and ITSReub generated the most informative (in term of peak number) and reproducible profiles and yielded a wider range of spacer sizes (134 to 1,387) than the other primer sets, which were limited in detecting long fragments. The minimum amount of DNA template and sensitivity in detection of minor DNA populations were evaluated with artificial mixtures of defined bacterial species. ITSF and ITSReub amplified all the bacteria at DNA template concentrations from 280 to 0.14 ng microl(-1), while the other primer sets failed to detect the spacers of one or more bacterial strains. Although the primer set consisting of ITSF and ITSReub and that of S-D-Bact-1522-b-S-20 and L-D-Bact-132-a-A-18 showed similar sensitivities for the DNA of Allorhizobium undicula mixed with the DNA of other species, the S-D-Bact-1522-b-S-20 and L-D-Bact-132-a-A-18 primer set failed to detect the DNA of Pseudomonas stutzeri.

                Author and article information

                Journal
                Environ Microbiol
                emi
                Environmental Microbiology
                Blackwell Publishing Ltd
                1462-2912
                1462-2920
                July 2011
                : 13
                : 7
                : 1815-1826
                Affiliations
                [1 ]simpleMicrobial Habitat Group, Max Planck Institute for Marine Microbiology Celsiusstrasse 1, 28359 Bremen, Germany
                [2 ]simpleCoral Reef Ecology Group (CORE), Leibniz Center for Tropical Marine Ecology Fahrenheitstrasse 6, 28359 Bremen, Germany
                [3 ]simpleMarine Science Station, Jordan University and Yarmouk University PO Box 195, 77110 Aqaba, Jordan
                Author notes
                For correspondence. *Email: christian.wild@ 123456zmt-bremen.de ; Tel. (+49) 421 30800 114; Fax (+49) 421 30800 30
                **E-mail: aramette@ 123456mpi-bremen.de ; Tel. (+49) 421 2028 863; Fax (+49) 421 2028 690
                [†]

                Present address: Department of Microbe-Plant Interactions, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Ingolstaedter Landstrasse 1, 85764 Neuherberg, Germany

                [‡]

                These authors contributed equally to this work.

                Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/onlineopen#OnlineOpen_Terms

                Article
                10.1111/j.1462-2920.2011.02494.x
                3207121
                21554515
                1c4344cb-b354-4311-b7d4-02a1481f24bd
                Copyright © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd

                Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation.

                History
                : 19 December 2010
                : 22 March 2011
                Categories
                Research Articles

                Microbiology & Virology
                Microbiology & Virology

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