The intestinal microbiome of fish under starvation

BackgroundStarvation not only affects the nutritional and health status of the animals, but also the microbial composition in the host’s intestine. Next-generation sequencing provides a unique opportunity to explore gut microbial communities and their interactions with hosts. However, studies on gut microbiomes have been conducted predominantly in humans and land animals. Not much is known on gut microbiomes of aquatic animals and their changes under changing environmental conditions. To address this shortcoming, we determined the microbial gene catalogue, and investigated changes in the microbial composition and host-microbe interactions in the intestine of Asian seabass in response to starvation.ResultsWe found 33 phyla, 66 classes, 130 orders and 278 families in the intestinal microbiome. Proteobacteria (48.8%), Firmicutes (15.3%) and Bacteroidetes (8.2%) were the three most abundant bacteria taxa. Comparative analyses of the microbiome revealed shifts in bacteria communities, with dramatic enrichment of Bacteroidetes, but significant depletion of Betaproteobacteria in starved intestines. In addition, significant differences in clusters of orthologous groups (COG) functional categories and orthologous groups were observed. Genes related to antibiotic activity in the microbiome were significantly enriched in response to starvation, and host genes related to the immune response were generally up-regulated.ConclusionsThis study provides the first insights into the fish intestinal microbiome and its changes under starvation. Further detailed study on interactions between intestinal microbiomes and hosts under dynamic conditions will shed new light on how the hosts and microbes respond to the changing environment.

[1]  P. Liu,et al.  Analysis of Stress-Responsive Transcriptome in the Intestine of Asian Seabass (Lates calcarifer) using RNA-Seq , 2013, DNA research : an international journal for rapid publication of reports on genes and genomes.

[2]  T. Shirakawa,et al.  Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. , 2009, FEMS immunology and medical microbiology.

[3]  Florent E. Angly,et al.  Microbial Ecology of Four Coral Atolls in the Northern Line Islands , 2008, PloS one.

[4]  Jo McEntyre,et al.  The NCBI Handbook , 2002 .

[5]  F. Dhabhar Enhancing versus Suppressive Effects of Stress on Immune Function: Implications for Immunoprotection and Immunopathology , 2009, Neuroimmunomodulation.

[6]  P. Kelly Nutrition, intestinal defence and the microbiome , 2010, Proceedings of the Nutrition Society.

[7]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[8]  L. Jourdonais,et al.  Effect of Gastric Mucin on Virulence of Bacteria in Intraperitoneal Injections in the Mouse , 1932 .

[9]  R. Knight,et al.  Worlds within worlds: evolution of the vertebrate gut microbiota , 2008, Nature Reviews Microbiology.

[10]  G. Weinstock The volatile microbiome , 2011, Genome Biology.

[11]  C. Quince,et al.  Environmental microbiology through the lens of high-throughput DNA sequencing: synopsis of current platforms and bioinformatics approaches. , 2012, Journal of microbiological methods.

[12]  J. Gilbert,et al.  Metagenomics - a guide from sampling to data analysis , 2012, Microbial Informatics and Experimentation.

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

[14]  Z. Bai,et al.  Analysis of the Asian Seabass Transcriptome Based on Expressed Sequence Tags , 2011, DNA research : an international journal for rapid publication of reports on genes and genomes.

[15]  V. Tremaroli,et al.  Functional interactions between the gut microbiota and host metabolism , 2012, Nature.

[16]  G. Macfarlane,et al.  Variation in human intestinal microbiota with age. , 2002, Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver.

[17]  Timothy L. Tickle,et al.  Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment , 2012, Genome Biology.

[18]  Robert G. Beiko,et al.  Identifying biologically relevant differences between metagenomic communities , 2010, Bioinform..

[19]  N. Wright,et al.  The effects of starvation and refeeding on intestinal cell proliferation in the mouse , 1984, Virchows Archiv. B, Cell pathology including molecular pathology.

[20]  I. Johnston Quantitative analysis of muscle breakdown during starvation in the marine flatfish Pleuronectes platessa , 2004, Cell and Tissue Research.

[21]  B. Cham,et al.  Importance of apolipoproteins in lipid metabolism. , 1978, Chemico-biological interactions.

[22]  R. Amann,et al.  Dual staining of natural bacterioplankton with 4',6-diamidino-2-phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16S rRNA sequences , 1992, Applied and environmental microbiology.

[23]  P. Bork,et al.  A human gut microbial gene catalogue established by metagenomic sequencing , 2010, Nature.

[24]  R. Jost,et al.  Biochemical Characterization of Two Wheat Phosphoethanolamine N-Methyltransferase Isoforms with Different Sensitivities to Inhibition by Phosphatidic Acid* , 2009, The Journal of Biological Chemistry.

[25]  D. Stahl,et al.  Monitoring the enrichment and isolation of sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16S rRNA sequences , 1993, Applied and environmental microbiology.

[26]  P. Verma,et al.  Starvation-Induced Impairment of Metabolism in a Freshwater Catfish , 2003, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[27]  J. Gilbert,et al.  Microbial metagenomics: beyond the genome. , 2011, Annual review of marine science.

[28]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[29]  R. Knight,et al.  Moving pictures of the human microbiome , 2011, Genome Biology.

[30]  J. Prosser,et al.  Establishment of Normal Gut Microbiota Is Compromised under Excessive Hygiene Conditions , 2011, PloS one.

[31]  M. Yamazaki,et al.  Microbiota-derived lactate accelerates colon epithelial cell turnover in starvation-refed mice , 2013, Nature Communications.

[32]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[33]  Rob Knight,et al.  Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. , 2012, Cell host & microbe.

[34]  W. L. Montgomery,et al.  Gut anatomy and pH in a red sea surgeonfish, Acanthurus nigrofuscus , 1988 .

[35]  Umaporn Uawisetwathana,et al.  Validation of Reference Genes for Real-Time PCR of Reproductive System in the Black Tiger Shrimp , 2012, PloS one.

[36]  C. Baldwin FAO SPECIES IDENTIFICATION GUIDE FOR FISHERY PURPOSES. THE LIVING MARINE RESOURCES OF THE WESTERN CENTRAL PACIFIC , 2003, Copeia.

[37]  N. Bols,et al.  An evaluation of potential reference genes for stability of expression in two salmonid cell lines after infection with either Piscirickettsia salmonis or IPNV , 2010, BMC Research Notes.

[38]  P. Shi,et al.  Analysis of bacterial diversity in the intestine of grass carp (Ctenopharyngodon idellus) based on 16S rDNA gene sequences , 2010 .

[39]  J. Doré,et al.  Direct Analysis of Genes Encoding 16S rRNA from Complex Communities Reveals Many Novel Molecular Species within the Human Gut , 1999, Applied and Environmental Microbiology.

[40]  A. Macpherson,et al.  Interactions between commensal intestinal bacteria and the immune system , 2004, Nature Reviews Immunology.

[41]  C. Huttenhower,et al.  Metagenomic microbial community profiling using unique clade-specific marker genes , 2012, Nature Methods.

[42]  E. Murphy,et al.  Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models , 2010, Gut.

[43]  S. Blum,et al.  Intestinal microflora and homeostasis of the mucosal immune response: implications for probiotic bacteria? , 2003, Current issues in intestinal microbiology.

[44]  Miriam L. Land,et al.  Trace: Tennessee Research and Creative Exchange Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification Recommended Citation Prodigal: Prokaryotic Gene Recognition and Translation Initiation Site Identification , 2022 .

[45]  P. Kelly Conference on 'over-and Undernutrition: Challenges and Approaches' Symposium 4: Gut Function: Effects on Over-and Undernutrition Nutrition, Intestinal Defence and the Microbiome , 2022 .

[46]  Lynn K. Carmichael,et al.  A Genomic View of the Human-Bacteroides thetaiotaomicron Symbiosis , 2003, Science.

[47]  Christian Munck,et al.  Functional Metagenomic Investigations of the Human Intestinal Microbiota , 2011, Front. Microbio..

[48]  Rob Knight,et al.  Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation , 2009, Proceedings of the National Academy of Sciences.

[49]  E. Koonin 22. The Clusters of Orthologous Groups (COGs) Database: Phylogenetic Classification of Proteins from Complete Genomes , 2003 .

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

[51]  Mukesh Jain,et al.  NGS QC Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data , 2012, PloS one.

[52]  Guozhu Liu,et al.  Expression analysis of immune-relevant genes in the spleen of large yellow croaker (Pseudosciaena crocea) stimulated with poly I:C. , 2006, Fish & shellfish immunology.

[53]  Yanping Wang,et al.  Human intestinal bacteria as reservoirs for antibiotic resistance genes. , 2004, Trends in microbiology.

[54]  J. Tap,et al.  Differential Adaptation of Human Gut Microbiota to Bariatric Surgery–Induced Weight Loss , 2010, Diabetes.

[55]  Benjamin P. Westover,et al.  Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont , 2005, Science.

[56]  J. Xia,et al.  Identification and analysis of immune-related transcriptome in Asian seabass Lates calcarifer , 2010, BMC Genomics.

[57]  B. Roe,et al.  A core gut microbiome in obese and lean twins , 2008, Nature.

[58]  Levi Waldron,et al.  Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples , 2012, Genome Biology.

[59]  D. Relman,et al.  Assembly of the human intestinal microbiota. , 2006, Trends in ecology & evolution.

[60]  D. Bellwood,et al.  Histological effects of cyanide, stress and starvation on the intestinal mucosa of Pomacentrus coelestis, a marine aquarium fish species , 1995 .

[61]  We are what we eat: how the diet of infants affects their gut microbiome , 2012, Genome Biology.

[62]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[63]  J. Jansson,et al.  Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. , 2006, The Journal of antimicrobial chemotherapy.

[64]  P. Scully,et al.  Early Life Stress Alters Behavior, Immunity, and Microbiota in Rats: Implications for Irritable Bowel Syndrome and Psychiatric Illnesses , 2009, Biological Psychiatry.

[65]  K. Brown,et al.  Diet-Induced Dysbiosis of the Intestinal Microbiota and the Effects on Immunity and Disease , 2012, Nutrients.

[66]  M. Kleerebezem,et al.  Microbiome dynamics of human epidermis following skin barrier disruption , 2012, Genome Biology.

[67]  M. Icaza-Chávez,et al.  Gut microbiota in health and disease , 2013 .

[68]  Robert S Chapkin,et al.  A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response , 2012, Genome Biology.

[69]  P. Brown,et al.  Proteomic analysis of rainbow trout (Oncorhynchus mykiss) intestinal epithelia: physiological acclimation to short-term starvation. , 2013, Comparative biochemistry and physiology. Part D, Genomics & proteomics.

[70]  Kirsty Brown,et al.  Correction: Brown, K., et al. Diet-Induced Dysbiosis of the Intestinal Microbiota and the Effects on Immunity and Disease. Nutrients 2012, 4, 1095–1119 , 2012, Nutrients.

[71]  F. Bushman,et al.  Linking Long-Term Dietary Patterns with Gut Microbial Enterotypes , 2011, Science.

[72]  P. Turnbaugh,et al.  Microbial ecology: Human gut microbes associated with obesity , 2006, Nature.

[73]  Huanming Yang,et al.  De novo assembly of human genomes with massively parallel short read sequencing. , 2010, Genome research.

[74]  Rob Knight,et al.  Direct sequencing of the human microbiome readily reveals community differences , 2010, Genome Biology.

[75]  Howard Ochman,et al.  Comparative Metagenomics and Population Dynamics of the Gut Microbiota in Mother and Infant , 2010, Genome biology and evolution.

[76]  Alexander F. Auch,et al.  MEGAN analysis of metagenomic data. , 2007, Genome research.