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      Structural variability and niche differentiation in the rhizosphere and endosphere bacterial microbiome of field-grown poplar trees

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          Abstract

          Background

          The plant microbiome represents one of the key determinants of plant health and productivity by providing a plethora of functional capacities such as access to low-abundance nutrients, suppression of phytopathogens, and resistance to biotic and/or abiotic stressors. However, a robust understanding of the structural composition of the bacterial microbiome present in different plant microenvironments and especially the relationship between below-ground and above-ground communities has remained elusive. In this work, we addressed hypotheses regarding microbiome niche differentiation and structural stability of the bacterial communities within different ecological plant niches.

          Methods

          We sampled the rhizosphere soil, root, stem, and leaf endosphere of field-grown poplar trees ( Populus tremula × Populus alba) and applied 16S rRNA amplicon pyrosequencing to unravel the bacterial communities associated with the different plant habitats.

          Results

          We found that the structural variability of rhizosphere microbiomes in field-grown poplar trees ( P. tremula × P. alba) is much lower than that of the endosphere microbiomes. Furthermore, our data not only confirm microbiome niche differentiation reports at the rhizosphere soil–root interface but also clearly show additional fine-tuning and adaptation of the endosphere microbiome in the stem and leaf compartment. Each plant compartment represents an unique ecological niche for the bacterial communities . Finally, we identified the core bacterial microbiome associated with the different ecological niches of Populus.

          Conclusions

          Understanding the complex host–microbe interactions of Populus could provide the basis for the exploitation of the eukaryote–prokaryote associations in phytoremediation applications, sustainable crop production (bio-energy efficiency), and/or the production of secondary metabolites.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s40168-017-0241-2) contains supplementary material, which is available to authorized users.

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          Most cited references58

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          Pyrosequencing enumerates and contrasts soil microbial diversity.

          Estimates of the number of species of bacteria per gram of soil vary between 2000 and 8.3 million (Gans et al., 2005; Schloss and Handelsman, 2006). The highest estimate suggests that the number may be so large as to be impractical to test by amplification and sequencing of the highly conserved 16S rRNA gene from soil DNA (Gans et al., 2005). Here we present the use of high throughput DNA pyrosequencing and statistical inference to assess bacterial diversity in four soils across a large transect of the western hemisphere. The number of bacterial 16S rRNA sequences obtained from each site varied from 26,140 to 53,533. The most abundant bacterial groups in all four soils were the Bacteroidetes, Betaproteobacteria and Alphaproteobacteria. Using three estimators of diversity, the maximum number of unique sequences (operational taxonomic units roughly corresponding to the species level) never exceeded 52,000 in these soils at the lowest level of dissimilarity. Furthermore, the bacterial diversity of the forest soil was phylum rich compared to the agricultural soils, which are species rich but phylum poor. The forest site also showed far less diversity of the Archaea with only 0.009% of all sequences from that site being from this group as opposed to 4%-12% of the sequences from the three agricultural sites. This work is the most comprehensive examination to date of bacterial diversity in soil and suggests that agricultural management of soil may significantly influence the diversity of bacteria and archaea.
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            The gut bacteria of insects: nonpathogenic interactions.

            The diversity of the Insecta is reflected in the large and varied microbial communities inhabiting the gut. Studies, particularly with termites and cockroaches, have focused on the nutritional contributions of gut bacteria in insects living on suboptimal diets. The indigenous gut bacteria, however, also play a role in withstanding the colonization of the gut by non-indigenous species including pathogens. Gut bacterial consortia adapt by the transfer of plasmids and transconjugation between bacterial strains, and some insect species provide ideal conditions for bacterial conjugation, which suggests that the gut is a "hot spot" for gene transfer. Genomic analysis provides new avenues for the study of the gut microbial community and will reveal the molecular foundations of the relationships between the insect and its microbiome. In this review the intestinal bacteria is discussed in the context of developing our understanding of symbiotic relationships, of multitrophic interactions between insects and plant or animal host, and in developing new strategies for controlling insect pests.
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              Properties of bacterial endophytes and their proposed role in plant growth.

              Bacterial endophytes live inside plants for at least part of their life cycle. Studies of the interaction of endophytes with their host plants and their function within their hosts are important to address the ecological relevance of endophytes. The modulation of ethylene levels in plants by bacterially produced 1-aminocyclopropane-1-carboxylate deaminase is a key trait that enables interference with the physiology of the host plant. Endophytes with this capacity might profit from association with the plant, because colonization is enhanced. In turn, host plants benefit by stress reduction and increased root growth. This mechanism leads to the concept of 'competent' endophytes, defined as endophytes that are equipped with genes important for maintenance of plant-endophyte associations. The ecological role of these endophytes and their relevance for plant growth are discussed here.
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                Author and article information

                Contributors
                +32(0)11 26 82 64 , bram.beckers@uhasselt.be
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                23 February 2017
                23 February 2017
                2017
                : 5
                : 25
                Affiliations
                [1 ]ISNI 0000 0001 0604 5662, GRID grid.12155.32, Centre for Environmental Sciences, , Hasselt University, ; Agoralaan building D, B-3590 Diepenbeek, Belgium
                [2 ]ISNI 0000 0001 0930 2361, GRID grid.4514.4, Current address: Department of Biology, , Lund University, ; Ecology Building, SE-22 362 Lund, Sweden
                [3 ]ISNI 0000000104788040, GRID grid.11486.3a, Department of Plant Systems Biology, , VIB, ; Technologiepark 927, B-9052 Ghent, Belgium
                [4 ]ISNI 0000 0001 2069 7798, GRID grid.5342.0, Department of Plant Biotechnology and Bioinformatics, , UGent, ; Technologiepark 927, B-9052 Ghent, Belgium
                Article
                241
                10.1186/s40168-017-0241-2
                5324219
                28231859
                3ebe6c37-591a-493a-8985-78587d930876
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 11 October 2016
                : 3 February 2017
                Funding
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100003130, Fonds Wetenschappelijk Onderzoek;
                Award ID: G032912N
                Funded by: UHasselt Methusalem
                Award ID: 08M03VGRJ
                Funded by: FundRef http://dx.doi.org/10.13039/501100003130, Fonds Wetenschappelijk Onderzoek;
                Award ID: Post-doc grant
                Award ID: PhD grant
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                populus tremula × populus alba,bacterial microbiome,rhizosphere,endosphere,microbiome niche differentiation,16s rrna amplicon pyrosequencing

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