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      Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets

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          Abstract

          Background

          The constant increase of aquaculture production and wealthy seafood consumption has forced the industry to explore alternative and more sustainable raw aquafeed materials, and plant ingredients have been used to replace marine feedstuffs in many farmed fish. The objective of the present study was to assess whether plant-based diets can induce changes in the intestinal mucus proteome, gut autochthonous microbiota and disease susceptibility of fish, and whether these changes could be reversed by the addition of sodium butyrate to the diets. Three different trials were performed using the teleostean gilthead sea bream ( Sparus aurata) as model. In a first preliminary short-term trial, fish were fed with the additive (0.8%) supplementing a basal diet with low vegetable inclusion (D1) and then challenged with a bacteria to detect possible effects on survival. In a second trial, fish were fed with diets with greater vegetable inclusion levels (D2, D3) and the long-term effect of sodium butyrate at a lower dose (0.4%) added to D3 (D4 diet) was tested on the intestinal proteome and microbiome. In a third trial, the long-term effectiveness of sodium butyrate (D4) to prevent disease outcome after an intestinal parasite ( Enteromyxum leei) challenge was tested.

          Results

          The results showed that opposed forces were driven by dietary plant ingredients and sodium butyrate supplementation in fish diet. On the one hand, vegetable diets induced high parasite infection levels that provoked drops in growth performance, decreased intestinal microbiota diversity, induced the dominance of the Photobacterium genus, as well as altered the gut mucosal proteome suggesting detrimental effects on intestinal function. On the other hand, butyrate addition slightly decreased cumulative mortality after bacterial challenge, avoided growth retardation in parasitized fish, increased intestinal microbiota diversity with a higher representation of butyrate-producing bacteria and reversed most vegetable diet-induced changes in the gut proteome.

          Conclusions

          This integrative work gives insights on the pleiotropic effects of a dietary additive on the restoration of intestinal homeostasis and disease resilience, using a multifaceted approach.

          Electronic supplementary material

          The online version of this article (10.1186/s40168-017-0390-3) contains supplementary material, which is available to authorized users.

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          Most cited references122

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          Fast UniFrac: Facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data

          Next-generation sequencing techniques, and PhyloChip, have made simultaneous phylogenetic analyses of hundreds of microbial communities possible. Insight into community structure has been limited by the inability to integrate and visualize such vast datasets. Fast UniFrac overcomes these issues, allowing integration of larger numbers of sequences and samples into a single analysis. Its new array-based implementation offers orders of magnitude improvements over the original version. New 3D visualization of principal coordinates analysis (PCoA) results, with the option to view multiple coordinate axes simultaneously, provides a powerful way to quickly identify patterns that relate vast numbers of microbial communities. We demonstrate the potential of Fast UniFrac using examples from three data types: Sanger-sequencing studies of diverse free-living and animal-associated bacterial assemblages and from the gut of obese humans as they diet, pyrosequencing data integrated from studies of the human hand and gut, and PhyloChip data from a study of citrus pathogens. We show that a Fast UniFrac analysis using a reference tree recaptures patterns that could not be detected without considering phylogenetic relationships and that Fast UniFrac, coupled with BLAST-based sequence assignment, can be used to quickly analyze pyrosequencing runs containing hundreds of thousands of sequences, revealing patterns relating human and gut samples. Finally, we show that the application of Fast UniFrac to PhyloChip data could identify well-defined subcategories associated with infection. Together, these case studies point the way towards a broad range of applications and demonstrate some of the new features of Fast UniFrac.
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            Expanding the utilization of sustainable plant products in aquafeeds: a review

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              Evidence for a core gut microbiota in the zebrafish.

              Experimental analysis of gut microbial communities and their interactions with vertebrate hosts is conducted predominantly in domesticated animals that have been maintained in laboratory facilities for many generations. These animal models are useful for studying coevolved relationships between host and microbiota only if the microbial communities that occur in animals in lab facilities are representative of those that occur in nature. We performed 16S rRNA gene sequence-based comparisons of gut bacterial communities in zebrafish collected recently from their natural habitat and those reared for generations in lab facilities in different geographic locations. Patterns of gut microbiota structure in domesticated zebrafish varied across different lab facilities in correlation with historical connections between those facilities. However, gut microbiota membership in domesticated and recently caught zebrafish was strikingly similar, with a shared core gut microbiota. The zebrafish intestinal habitat therefore selects for specific bacterial taxa despite radical differences in host provenance and domestication status.
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                Author and article information

                Contributors
                carla.piazzon@csic.es
                j.calduch@csic.es
                Belen.Fouz@uv.es
                itziar.estensoro@csic.es
                paula.simo@csic.es
                mpuyalto@norel.net
                Vasilis.Karalazos@biomar.gr
                oswaldo.palenzuela@csic.es
                ariadna.sitja@csic.es
                jaime.perez.sanchez@csic.es
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                28 December 2017
                28 December 2017
                2017
                : 5
                : 164
                Affiliations
                [1 ]ISNI 0000 0004 1800 9433, GRID grid.452499.7, Fish Pathology Group, , Instituto de Acuicultura Torre de la Sal (IATS-CSIC), ; Castellón, Spain
                [2 ]ISNI 0000 0004 1800 9433, GRID grid.452499.7, Nutrigenomics and Fish Growth Endocrinology Group, , Instituto de Acuicultura Torre de la Sal (IATS-CSIC), ; Castellón, Spain
                [3 ]ISNI 0000 0001 2173 938X, GRID grid.5338.d, Department of Microbiology and Ecology, Faculty of Biology, , University of Valencia, ; Valencia, Spain
                [4 ]Norel S.A., Madrid, Spain
                [5 ]BioMar R&D, Grangemouth, UK
                Author information
                http://orcid.org/0000-0002-7473-3413
                Article
                390
                10.1186/s40168-017-0390-3
                5745981
                29282153
                4c530cf4-874c-4e72-b6b7-82cf9dbfb3cc
                © 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
                : 1 June 2017
                : 18 December 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100004963, Seventh Framework Programme;
                Award ID: 288925
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010678, H2020 Food;
                Award ID: 634429
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100007136, Secretaría de Estado de Investigación, Desarrollo e Innovación;
                Award ID: AGL2013-48560-C02-1-R
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100007136, Secretaría de Estado de Investigación, Desarrollo e Innovación;
                Award ID: AGL2013-48560-C02-1-R
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003339, Consejo Superior de Investigaciones Científicas;
                Award ID: 201740E013
                Award Recipient :
                Funded by: Generalitat Valenciana
                Award ID: APOSTD/2016/037
                Award Recipient :
                Funded by: Generalitat Valenciana
                Award ID: PROMETEOII/2014/085
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100007136, Secretaría de Estado de Investigación, Desarrollo e Innovación;
                Award ID: FPDI-2013-15741
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                sparus aurata,intestinal health,microbiome,proteome,sodium butyrate,nutrition,enteromyxum leei,myxozoa,photobacterium,pathogen challenge

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