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      Abundance determines the functional role of bacterial phylotypes in complex communities

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          Abstract

          Bacterial communities are essential for the functioning of the Earth's ecosystems 1. A key challenge is to quantify the functional roles of bacterial taxa in nature to understand how the properties of ecosystems change over time or under different environmental conditions 2. Such knowledge could be used, for example, to understand how bacteria modulate biogeochemical cycles 3, and to engineer bacterial communities to optimise desirable functional processes 4. Communities of bacteria are, however, extraordinarily complex with hundreds of interacting taxa in every gram of soil and every millilitre of pond water 5. Little is known about how the tangled interactions within natural bacterial communities mediate ecosystem functioning, but high levels of bacterial diversity have led to the assumption that many taxa are functionally redundant 6. Here, we pinpointed the bacterial taxa associated with keystone functional roles, and show that rare and common bacteria are implicated in fundamentally different types of ecosystem functioning. By growing hundreds of bacterial communities collected from a natural aquatic environment (rainwater-filled tree holes) under the same environmental conditions, we show that negative statistical interactions among abundant phylotypes drove variation in broad functional measures (respiration, metabolic potential, cell yield), while positive interactions between rare phylotypes influenced narrow functional measures (the capacity of the communities to degrade specific substrates). The results alter our understanding of bacterial ecology by demonstrating that unique components of complex communities are associated with different types of ecosystem functioning.

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          Most cited references23

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          Microbial control over carbon cycling in soil

          A major thrust of terrestrial microbial ecology is focused on understanding when and how the composition of the microbial community affects the functioning of biogeochemical processes at the ecosystem scale (meters-to-kilometers and days-to-years). While research has demonstrated these linkages for physiologically and phylogenetically “narrow” processes such as trace gas emissions and nitrification, there is less conclusive evidence that microbial community composition influences the “broad” processes of decomposition and organic matter (OM) turnover in soil. In this paper, we consider how soil microbial community structure influences C cycling. We consider the phylogenetic level at which microbes form meaningful guilds, based on overall life history strategies, and suggest that these are associated with deep evolutionary divergences, while much of the species-level diversity probably reflects functional redundancy. We then consider under what conditions it is possible for differences among microbes to affect process dynamics, and argue that while microbial community structure may be important in the rate of OM breakdown in the rhizosphere and in detritus, it is likely not important in the mineral soil. In mineral soil, physical access to occluded or sorbed substrates is the rate-limiting process. Microbial community influences on OM turnover in mineral soils are based on how organisms allocate the C they take up – not only do the fates of the molecules differ, but they can affect the soil system differently as well. For example, extracellular enzymes and extracellular polysaccharides can be key controls on soil structure and function. How microbes allocate C may also be particularly important for understanding the long-term fate of C in soil – is it sequestered or not?
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            The contribution of species richness and composition to bacterial services.

            Bacterial communities provide important services. They break down pollutants, municipal waste and ingested food, and they are the primary means by which organic matter is recycled to plants and other autotrophs. However, the processes that determine the rate at which these services are supplied are only starting to be identified. Biodiversity influences the way in which ecosystems function, but the form of the relationship between bacterial biodiversity and functioning remains poorly understood. Here we describe a manipulative experiment that measured how biodiversity affects the functioning of communities containing up to 72 bacterial species constructed from a collection of naturally occurring culturable bacteria. The experimental design allowed us to manipulate large numbers of bacterial species selected at random from those that were culturable. We demonstrate that there is a decelerating relationship between community respiration and increasing bacterial diversity. We also show that both synergistic interactions among bacterial species and the composition of the bacterial community are important in determining the level of ecosystem functioning.
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              Competition, not cooperation, dominates interactions among culturable microbial species.

              Microbial cells secrete numerous enzymes, scavenging molecules, and signals that can promote the growth and survival of other cells around them [1-4]. This observation is consistent with the evolution of cooperation within species [5], and there is now an increasing emphasis on the importance of cooperation between different microbial species [4, 6]. We lack, however, a systematic test of the importance of mutually positive interactions between different species, which is vital for assessing the commonness and importance of cooperative evolution in natural communities. Here, we study the extent of mutually positive interaction among bacterial strains isolated from a common aquatic environment. Using data collected from two independent experiments evaluating community productivity across diversity gradients, we show that (1) in pairwise species combinations, the great majority of interactions are net negative and (2) there is no evidence that strong higher-order positive effects arise when more than two species are mixed together. Our data do not exclude the possibility of positive effects in one direction where one species gains at the expense of another, i.e., predator-prey-like interactions. However, these do not constitute cooperation and our analysis suggests that the typical result of adaptation to other microbial species will be competitive, rather than cooperative, phenotypes. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                101674869
                44774
                Nat Microbiol
                Nat Microbiol
                Nature microbiology
                2058-5276
                18 June 2018
                18 June 2018
                July 2018
                18 December 2018
                : 3
                : 7
                : 767-772
                Affiliations
                [1 ]Department of Life Sciences, Silwood Park Campus, Imperial College London, Buckhurst Road, Ascot, SL5 7PY
                Author notes
                [* ] Correspondence. Thomas Bell, thomas.bell@ 123456imperial.ac.uk
                [2]

                Current address: Division of Biology and Conservation Ecology, School of Science and the Environment, Manchester Metropolitan University, Manchester, UK

                Article
                EMS77807
                10.1038/s41564-018-0180-0
                6065991
                29915204
                f8be4a25-67db-461a-9149-c0578906a63f

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                Categories
                Article

                functional interactions,microbiome,biodiversity,ecosystem functioning

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