Host-microbiota interactions and responses to grass carp reovirus infection in Ctenopharyngodon idellus.

Gut microbiota could facilitate host to defense diseases, but fish-microbiota interactions during viral infection and the underlying mechanism are poorly understood. We examined interactions and responses of gut microbiota to grass carp reovirus (GCRV) infection in Ctenopharyngodon idellus, which is the most important aquaculture fish worldwide. We found that GCRV infection group with serious hemorrhagic symptoms (G7s) showed considerably different gut microbiota, especially with an abnormally high abundance of gram-negative anaerobic Cetobacterium somerae. It also showed the lowest (p < 0.05) alpha-diversity but with much higher ecological process of homogenizing dispersal (28.8%), confirming a dysbiosis of the gut microbiota after viral infection. Interestingly, signaling pathways of NOD-like receptors (NLRs), toll-like receptors (TLRs), and lipopolysaccharide (LPS) stimulation genes were significantly (q-value < 0.01) enriched in G7s, which also significantly (p < 0.01) correlated with the core gut microbial genera of Cetobacterium and Acinetobacter. The results suggested that an expansion of C. somerae initiated by GCRV could aggravate host inflammatory reactions through the LPS-related NLRs and TLRs pathways. This study advances our understanding of the interplay between fish immunity and gut microbiota challenged by viruses, it also sheds new insights for ecological defense of fish diseases with the help of gut microbiota. This article is protected by copyright. All rights reserved.

[1]  J. Rawls,et al.  Commensal Microbiota Regulate Vertebrate Innate Immunity-Insights From the Zebrafish , 2019, Front. Immunol..

[2]  Zuoyan Zhu,et al.  Different responses in one‐year‐old and three‐year‐old grass carp reveal the mechanism of age restriction of GCRV infection , 2019, Fish & shellfish immunology.

[3]  J. Romero,et al.  Cetobacterium Is a Major Component of the Microbiome of Giant Amazonian Fish (Arapaima gigas) in Ecuador , 2018, Animals : an open access journal from MDPI.

[4]  L. Navar,et al.  Inflammation as a Regulator of the Renin-Angiotensin System and Blood Pressure , 2018, Current Hypertension Reports.

[5]  C. Lozupone,et al.  Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. , 2018, Current opinion in microbiology.

[6]  J. Xiong,et al.  Current understanding on the roles of gut microbiota in fish disease and immunity , 2018, Zoological research.

[7]  Q. Yan,et al.  Comparative study on the gut microbiotas of four economically important Asian carp species , 2018, Science China Life Sciences.

[8]  I. Babiak,et al.  Low incubation temperature during early development negatively affects survival and related innate immune processes in zebrafish larvae exposed to lipopolysaccharide , 2018, Scientific Reports.

[9]  Ping Chen,et al.  Transcriptome Analysis of Epithelioma Papulosum Cyprini Cells Infected by Reovirus Isolated from Allogynogenetic Silver Crucian Carp , 2018, Viruses.

[10]  Li Nie,et al.  Interplay between the gut microbiota and immune responses of ayu (Plecoglossus altivelis) during Vibrio anguillarum infection , 2017, Fish & shellfish immunology.

[11]  Fan Xiong,et al.  Succession and Fermentation Products of Grass Carp (Ctenopharyngodon idellus) Hindgut Microbiota in Response to an Extreme Dietary Shift , 2017, Front. Microbiol..

[12]  Jiabao Li,et al.  Changes in the Intestinal Microbiota of Gibel Carp (Carassius gibelio) Associated with Cyprinid herpesvirus 2 (CyHV-2) Infection , 2017, Current Microbiology.

[13]  Benjamin M Hillmann,et al.  BugBase predicts organism-level microbiome phenotypes , 2017, bioRxiv.

[14]  M. Dessing,et al.  Depletion of Gut Microbiota Protects against Renal Ischemia-Reperfusion Injury. , 2017, Journal of the American Society of Nephrology : JASN.

[15]  B. Bohannan,et al.  The role of adaptive immunity as an ecological filter on the gut microbiota in zebrafish , 2017, The ISME Journal.

[16]  A. Figueras,et al.  Conserved gene regulation during acute inflammation between zebrafish and mammals , 2017, Scientific Reports.

[17]  L. Weyrich,et al.  Embracing the gut microbiota: the new frontier for inflammatory and infectious diseases , 2017, Clinical & translational immunology.

[18]  Jizhong Zhou,et al.  Environmental filtering decreases with fish development for the assembly of gut microbiota. , 2016, Environmental microbiology.

[19]  C. Jackson,et al.  Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown , 2016, Molecular ecology.

[20]  Xiaoyan Xu,et al.  Transcriptome Analysis of the Innate Immunity-Related Complement System in Spleen Tissue of Ctenopharyngodon idella Infected with Aeromonas hydrophila , 2016, PloS one.

[21]  W. Garrett,et al.  Gut microbiota, metabolites and host immunity , 2016, Nature Reviews Immunology.

[22]  L. Zhong,et al.  Characterization of grass carp spleen transcriptome during GCRV infection. , 2016, Genetics and molecular research : GMR.

[23]  James Kinross,et al.  The gut microbiota and host health: a new clinical frontier , 2015, Gut.

[24]  Qiong Luo,et al.  The draft genome of the grass carp (Ctenopharyngodon idellus) provides insights into its evolution and vegetarian adaptation , 2015, Nature Genetics.

[25]  Jianguo Su,et al.  Insights into the Antiviral Immunity against Grass Carp (Ctenopharyngodon idella) Reovirus (GCRV) in Grass Carp , 2015, Journal of immunology research.

[26]  J. Ni,et al.  Comparative study on gastrointestinal microbiota of eight fish species with different feeding habits , 2014, Journal of applied microbiology.

[27]  D. Post,et al.  Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch) , 2014, Ecology letters.

[28]  Q. Yan,et al.  Factors influencing the grass carp gut microbiome and its effect on metabolism. , 2014, FEMS microbiology ecology.

[29]  S. Winter,et al.  Why related bacterial species bloom simultaneously in the gut: principles underlying the ‘Like will to like’ concept , 2014, Cellular microbiology.

[30]  S. Meri.  Complement activation in diseases presenting with thrombotic microangiopathy. , 2013, European journal of internal medicine.

[31]  Gabriel Núñez,et al.  Control of pathogens and pathobionts by the gut microbiota , 2013, Nature Immunology.

[32]  Zihua Hu,et al.  Gut Microbiota Contributes to the Growth of Fast-Growing Transgenic Common Carp (Cyprinus carpio L.) , 2013, PloS one.

[33]  Z. Sha,et al.  Class II, major histocompatibility complex, transactivator (CIITA) in channel catfish: identification and expression patterns responding to different pathogens , 2012, Molecular Biology Reports.

[34]  Steven D. Essinger,et al.  Environmental and ecological factors that shape the gut bacterial communities of fish: a meta‐analysis , 2012, Molecular ecology.

[35]  J. Clemente,et al.  The Impact of the Gut Microbiota on Human Health: An Integrative View , 2012, Cell.

[36]  S. Wu,et al.  Composition, Diversity, and Origin of the Bacterial Community in Grass Carp Intestine , 2012, PloS one.

[37]  N. Roher,et al.  PAMPs, PRRs and the genomics of gram negative bacterial recognition in fish. , 2011, Developmental and comparative immunology.

[38]  Michael Klompas,et al.  Acinetobacter baumannii: An Emerging and Important Pathogen. , 2010, Journal of clinical outcomes management : JCOM.

[39]  B. Finlay,et al.  Gut microbiota in health and disease. , 2010, Physiological reviews.

[40]  J. Balcázar,et al.  Host–microbiota interactions within the fish intestinal ecosystem , 2010, Mucosal Immunology.

[41]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[42]  J. Balcázar,et al.  A review on the interactions between gut microbiota and innate immunity of fish. , 2008, FEMS immunology and medical microbiology.

[43]  H. Sugita,et al.  Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish , 2007, Letters in applied microbiology.

[44]  S. Girardin,et al.  Nod‐like receptors in innate immunity and inflammatory diseases , 2007, Annals of medicine.

[45]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[46]  X. de Lamballerie,et al.  Sequence of genome segments 1, 2, and 3 of the grass carp reovirus (Genus Aquareovirus, family Reoviridae). , 2000, Biochemical and biophysical research communications.

[47]  Qianqian Zhang,et al.  Comparative Analysis of the Intestinal Bacterial Communities in Different Species of Carp by Pyrosequencing , 2014, Microbial Ecology.

[48]  Carly L. Daniels,et al.  Microbial manipulations to improve fish health and production--a Mediterranean perspective. , 2011, Fish & shellfish immunology.

[49]  E. Mittge,et al.  Evidence for a core gut microbiota in the zebrafish , 2011, The ISME Journal.

[50]  Yulin Jiang,et al.  Hemorrhagic Disease of Grass Carp: Status of Outbreaks, Diagnosis, Surveillance, and Research , 2009 .

[51]  P. Lawson,et al.  Cetobacterium somerae sp. nov. from human feces and emended description of the genus Cetobacterium. , 2003, Systematic and applied microbiology.