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      Probiotic Diversity Enhances Rhizosphere Microbiome Function and Plant Disease Suppression

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          ABSTRACT

          Bacterial communities associated with plant roots play an important role in the suppression of soil-borne pathogens, and multispecies probiotic consortia may enhance disease suppression efficacy. Here we introduced defined Pseudomonas species consortia into naturally complex microbial communities and measured the importance of Pseudomonas community diversity for their survival and the suppression of the bacterial plant pathogen Ralstonia solanacearum in the tomato rhizosphere microbiome. The survival of introduced Pseudomonas consortia increased with increasing diversity. Further, high Pseudomonas diversity reduced pathogen density in the rhizosphere and decreased the disease incidence due to both intensified resource competition and interference with the pathogen. These results provide novel mechanistic insights into elevated pathogen suppression by diverse probiotic consortia in naturally diverse plant rhizospheres. Ecologically based community assembly rules could thus play a key role in engineering functionally reliable microbiome applications.

          IMPORTANCE

          The increasing demand for food supply requires more-efficient control of plant diseases. The use of probiotics, i.e., naturally occurring bacterial antagonists and competitors that suppress pathogens, has recently reemerged as a promising alternative to agrochemical use. It is, however, still unclear how many and which strains we should choose for constructing effective probiotic consortia. Here we present a general ecological framework for assembling effective probiotic communities based on in vitro characterization of community functioning. Specifically, we show that increasing the diversity of probiotic consortia enhances community survival in the naturally diverse rhizosphere microbiome, leading to increased pathogen suppression via intensified resource competition and interference with the pathogen. We propose that these ecological guidelines can be put to the test in microbiome engineering more widely in the future.

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          Most cited references31

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          Microbial diversity determines the invasion of soil by a bacterial pathogen.

          Natural ecosystems show variable resistance to invasion by alien species, and this resistance can relate to the species diversity in the system. In soil, microorganisms are key components that determine life support functions, but the functional redundancy in the microbiota of most soils has long been thought to overwhelm microbial diversity-function relationships. We here show an inverse relationship between soil microbial diversity and survival of the invading species Escherichia coli O157:H7, assessed by using the marked derivative strain T. The invader's fate in soil was determined in the presence of (i) differentially constructed culturable bacterial communities, and (ii) microbial communities established using a dilution-to-extinction approach. Both approaches revealed a negative correlation between the diversity of the soil microbiota and survival of the invader. The relationship could be explained by a decrease in the competitive ability of the invader in species-rich vs. species-poor bacterial communities, reflected in the amount of resources used and the rate of their consumption. Soil microbial diversity is a key factor that controls the extent to which bacterial invaders can establish.
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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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              Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: a systematic review of randomized controlled trials

              Background The effects of probiotic supplementation on fecal microbiota composition in healthy adults have not been well established. We aimed to provide a systematic review of the potential evidence for an effect of probiotic supplementation on the composition of human fecal microbiota as assessed by high-throughput molecular approaches in randomized controlled trials (RCTs) of healthy adults. Methods The survey of peer-reviewed papers was performed on 17 August 2015 by a literature search through PubMed, SCOPUS, and ISI Web of Science. Additional papers were identified by checking references of relevant papers. Search terms included healthy adult, probiotic, bifidobacterium, lactobacillus, gut microbiota, fecal microbiota, intestinal microbiota, intervention, and (clinical) trial. RCTs of solely probiotic supplementation and placebo in healthy adults that examined alteration in composition of overall fecal microbiota structure assessed by shotgun metagenomic sequencing, 16S ribosomal RNA sequencing, or phylogenetic microarray methods were included. Independent collection and quality assessment of studies were performed by two authors using predefined criteria including methodological quality assessment of reports of the clinical trials based on revised tools from PRISMA/Cochrane and by the Jadad score. Results Seven RCTs investigating the effect of probiotic supplementation on fecal microbiota in healthy adults were identified and included in the present systematic review. The quality of the studies was assessed as medium to high. Still, no effects were observed on the fecal microbiota composition in terms of α-diversity, richness, or evenness in any of the included studies when compared to placebo. Only one study found that probiotic supplementation significantly modified the overall structure of the fecal bacterial community in terms of β-diversity when compared to placebo. Conclusions This systematic review of the pertinent literature demonstrates a lack of evidence for an impact of probiotics on fecal microbiota composition in healthy adults. Future studies would benefit from pre-specifying the primary outcome and transparently reporting the results including effect sizes, confidence intervals, and P values as well as providing a clear distinction of between-group and within-group comparisons.
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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                13 December 2016
                Nov-Dec 2016
                : 7
                : 6
                : e01790-16
                Affiliations
                [a ]Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing, People’s Republic of China
                [b ]Utrecht University, Institute for Environmental Biology, Ecology and Biodiversity, Utrecht, the Netherlands
                [c ]Department of Biology, University of York, Wentworth Way, York, United Kingdom
                [d ]German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
                [e ]Leipzig University, Institute of Biology, Leipzig, Germany
                Author notes
                Address correspondence to Zhong Wei, weizhong@ 123456njau.edu.cn , or Yang-chun Xu, ycxu@ 123456njau.edu.cn .

                J.H. and Z.W. contributed equally to this article.

                Editor Nicole Dubilier, Max Planck Institute for Marine Microbiology

                Article
                mBio01790-16
                10.1128/mBio.01790-16
                5156302
                27965449
                588520a2-0c41-49ea-9886-5a1b2ff1e51b
                Copyright © 2016 Hu et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 29 September 2016
                : 14 November 2016
                Page count
                supplementary-material: 5, Figures: 3, Tables: 2, Equations: 0, References: 44, Pages: 8, Words: 7791
                Funding
                This work, including the efforts of Qi-rong Shen, was funded by the National Key Basic Research Program of China (2015CB150503), the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, and the 111 project (B12009). This work, including the efforts of Zhong Wei, was funded by National Natural Science Foundation of China (NSFC) (41301262 and 41671248), Young Elite Scientist Sponsorship Program by CAST (2015QNRC001), and the Qing Lan Project. This work, including the efforts of Yangchun Xu, was funded by National Natural Science Foundation of China (NSFC) (41471213) and the Qing Lan Project. This work, including the efforts of Alexandre Jousset, was funded by Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO) (ALW.870.15.050) and the Koninklijke Nederlandse Akademie van Wetenschappen (530-5CDP18). This work, including the efforts of Ville Friman, was funded by British Ecological Society (BES) (105624) and the Wellcome Trust (reference no. 105624) through the Centre for Chronic Diseases and Disorders (C2D2) at the University of York.
                Categories
                Research Article
                Custom metadata
                November/December 2016

                Life sciences
                Life sciences

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