The intestinal microbiome of fish under starvation

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Xia, Jun H ^a   Lin, Grace ^a   Fu, Gui H ^a   Wan, Zi Y ^a   Lee, May ^a   Wang, Le ^a   Liu, Xiao J ^a   Yue, Gen H ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Fish; Interaction; Microbiome; Nutrition; Starvation; Stress

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENE; BACTEROIDETES; CONTROLLED STUDY; FIRMICUTES; FISH; GENETIC ANALYSIS; HOST PATHOGEN INTERACTION; INTESTINE FLORA; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIOME; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEOBACTERIA; SPECIES COMPOSITION; STARVATION; UNINDEXED SEQUENCE;

ANIMALIA; BACTEROIDETES; BETAPROTEOBACTERIA; FIRMICUTES; PROTEOBACTERIA;

ANIMALS; BIODIVERSITY; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; FISHES; GENE EXPRESSION PROFILING; GENE-ENVIRONMENT INTERACTION; INTESTINES; METAGENOME; MICROBIOTA; MOLECULAR SEQUENCE DATA; NUTRITIONAL STATUS; PHYLOGENY; RNA, RIBOSOMAL, 16S; STARVATION;

EID: 84898047118     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-266     Document Type: Article

References (74)

1. Okada T, Fukuda S, Hase K, Nishiumi S, Izumi Y, Yoshida M, Hagiwara T, Kawashima R, Yamazaki M, Oshio T, Otsubo T, Inagaki-Ohara K, Kakimoto K, Higuchi K, Kawamura YI, Ohno H, Dohi T. Microbiota-derived lactate accelerates colon epithelial cell turnover in starvation-refed mice. Nat Commun 2013, 4:1654.
2. Furet JP, Kong LC, Tap J, Poitou C, Basdevant A, Bouillot JL, Mariat D, Corthier G, Doré J, Henegar C, Rizkalla S, Clément K. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 2010, 59(12):3049-3057. 10.2337/db10-0253, 2992765, 20876719.
3. Goodlad RA, Wright NA. The effects of starvation and refeeding on intestinal cell proliferation in the mouse. Virchows Arch B Cell Pathol Incl Mol Pathol 1984, 45(1):63-73. 10.1007/BF02889852, 6142558.
4. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature 2006, 444(7122):1022-1023. 10.1038/4441022a, 17183309.
5. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012, 489(7415):242-249. 10.1038/nature11552, 22972297.
6. Moore AM, Munck C, Sommer MO, Dantas G. Functional metagenomic investigations of the human intestinal microbiota. Front Microbiol 2011, 2:188. 3195301, 22022321.
7. Kelly P. Symposium 4: Gut function: effects on over- and undernutrition nutrition, intestinal defence and the microbiome. Proc Nutr Soc 2010, 69(2):261-268. 10.1017/S0029665110000108, 20202280.
8. O'Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009, 65(3):263-267.
9. Tanaka S, Kobayashi T, Songjinda P, Tateyama A, Tsubouchi M, Kiyohara C, Shirakawa T, Sonomoto K, Nakayama J. Influence of antibiotic exposure in the early postnatal period on the development of intestinal microbiota. Fems Immunol Med Mic 2009, 56(1):80-87.
10. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, Sogin ML, Jones WJ, Roe BA, Affourtit JP, Egholm M, Henrissat B, Heath AC, Knight R, Gordon JI. A core gut microbiome in obese and lean twins. Nature 2009, 457(7228):480-484. 10.1038/nature07540, 2677729, 19043404.
11. Hopkins MJ, Sharp R, Macfarlane GT. Variation in human intestinal microbiota with age. Digest Liver Dis 2002, 34:S12-S18.
12. Schmidt B, Mulder IE, Musk CC, Aminov RI, Lewis M, Stokes CR, Bailey M, Prosser JI, Gill BP, Pluske JR, Kelly D. Establishment of normal gut microbiota is compromised under excessive hygiene conditions. Plos One 2011, 6(12):e28284. 10.1371/journal.pone.0028284, 3229561, 22164261.
13. Dethlefsen L, Eckburg PB, Bik EM, Relman DA. Assembly of the human intestinal microbiota. Trends Ecol Evol 2006, 21(9):517-523. 10.1016/j.tree.2006.06.013, 16820245.
14. Brown K, DeCoffe D, Molcan E, Gibson DL. Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease. Nutrients 2012, 4(11):1552-1553.
15. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012, 13(9):R79. 10.1186/gb-2012-13-9-r79, 3506950, 23013615.
16. Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, Knights D, Gajer P, Ravel J, Fierer N, Gordon JI, Knight R. Moving pictures of the human microbiome. Genome Biol 2011, 12(5):R50. 10.1186/gb-2011-12-5-r50, 3271711, 21624126.
17. Kuczynski J, Costello EK, Nemergut DR, Zaneveld J, Lauber CL, Knights D, Koren O, Fierer N, Kelley ST, Ley RE, Gordon JI, Knight R. Direct sequencing of the human microbiome readily reveals community differences. Genome Biol 2010, 11(5):210. 10.1186/gb-2010-11-5-210, 2898070, 20441597.
18. Ponten TS. Metatranscriptomics of the human gut microbiome. Genome Biol 2011, 12:3-3.
19. Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, Huttenhower C, Izard J. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol 2012, 13(6):R42. 10.1186/gb-2012-13-6-r42, 3446314, 22698087.
20. Weinstock GM. The volatile microbiome. Genome Biol 2011, 12(5):114. 10.1186/gb-2011-12-5-114, 3219960, 21635714.
21. Zeeuwen P, Boekhorst J, van den Bogaard EH, de Koning HD, van de Kerkhof PMC, Saulnier DM, van Swam II, van Hijum S, Kleerebezem M, Schalkwijk J, Timmerman HM. Microbiome dynamics of human epidermis following skin barrier disruption. Genome Biol 2012, 13(11):R101. 10.1186/gb-2012-13-11-r101, 3580493, 23153041.
22. Vaishampayan PA, Kuehl JV, Froula JL, Morgan JL, Ochman H, Francino MP. Comparative metagenomics and population dynamics of the gut microbiota in mother and infant. Genome Biol Evol 2010, 2:53-66. 10.1093/gbe/evp057, 2839348, 20333224.
23. Thomas T, Gilbert J, Meyer F. Metagenomics - a guide from sampling to data analysis. Microb Inform Exp 2012, 2(1):3. 10.1186/2042-5783-2-3, 3351745, 22587947.
24. Han SF, Liu YC, Zhou ZG, He SX, Cao YA, Shi PJ, Yao B, Ringo E. Analysis of bacterial diversity in the intestine of grass carp (Ctenopharyngodon idellus) based on 16S rDNA gene sequences. Aquac Res 2010, 42(1):47-56.
25. Wu S, Wang G, Angert ER, Wang W, Li W, Zou H. Composition, diversity, and origin of the bacterial community in grass carp intestine. Plos One 2012, 7(2):e30440. 10.1371/journal.pone.0030440, 3282688, 22363439.
26. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF. Evidence for a core gut microbiota in the zebrafish. ISME J 2011, 5(10):1595-1608. 10.1038/ismej.2011.38, 3176511, 21472014.
27. Larson H. Order Perciformes. Suborder Percoidei. Centropomidae. Sea perches. FAO species identification guide for fishery purposes The living marine resources of the Western Central Pacific 1999, 4:2429-2432. Rome: FAO, Carpenter KE, Niem VH.
28. Gilbert JA, Dupont CL. Microbial metagenomics: beyond the genome. Annu Rev Mar Sci 2011, 3:347-371.
29. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 2012, 9(8):811. 10.1038/nmeth.2066, 3443552, 22688413.
30. Pop M. We are what we eat: how the diet of infants affects their gut microbiome. Genome Biol 2012, 13(4):152. 10.1186/gb-2012-13-4-152, 3446294, 22546514.
31. Schwartz S, Friedberg I, Ivanov IV, Davidson LA, Goldsby JS, Dahl DB, Herman D, Wang M, Donovan SM, Chapkin RS. A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biol 2012, 13(4):R32. 10.1186/gb-2012-13-4-r32, 3446306, 22546241.
32. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010, 464(7285):59-65. 10.1038/nature08821, 3779803, 20203603.
33. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 2008, 6(10):776-788. 10.1038/nrmicro1978, 2664199, 18794915.
34. Crawford PA, Crowley JR, Sambandam N, Muegge BD, Costello EK, Hamady M, Knight R, Gordon JI. Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci U S A 2009, 106(27):11276-11281. 10.1073/pnas.0902366106, 2700149, 19549860.
35. Murphy EF, Cotter PD, Healy S, Marques TM, O'Sullivan O, Fouhy F, Clarke SF, O'Toole PW, Quigley EM, Stanton C, Ross PR, O'Doherty RM, Shanahan F. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 2010, 59:1635-1642. 10.1136/gut.2010.215665, 20926643.
36. Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 2003, 299(5615):2074-2076. 10.1126/science.1080029, 12663928.
37. Salyers AA, Gupta A, Wang YP. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol 2004, 12(9):412-416. 10.1016/j.tim.2004.07.004, 15337162.
38. Lofmark S, Jernberg C, Jansson JK, Edlund C. Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J Antimicrob Chemoth 2006, 58(6):1160-1167.
39. Semova I, Carten JD, Stombaugh J, Mackey LC, Knight R, Farber SA, Rawls JF. Microbiota regulate intestinal absorption and metabolism of fatty acids in the zebrafish. Cell host microbe 2012, 12(3):277-288. 10.1016/j.chom.2012.08.003, 3517662, 22980325.
40. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li HZ, Bushman FD, Lewis JD. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011, 333(6052):105-108.
41. Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinforma 2010, 11:119.
42. Koonin EV. The Clusters of Orthologous Groups (COGs) Database: phylogenetic classification of proteins from complete genomes. The NCBI Handbook 2002, Bethesda (MD): National Center for Biotechnology Information (US), McEntyre J, Ostell J.
43. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev 2010, 90(3):859-904. 10.1152/physrev.00045.2009, 20664075.
44. Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, Buhler JD, Gordon JI. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 2005, 307(5717):1955-1959. 10.1126/science.1109051, 15790854.
45. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004, 4(6):478-485. 10.1038/nri1373, 15173836.
46. Tripathi G, Verma P. Starvation-induced impairment of metabolism in a freshwater catfish. Z Naturforsch C 2003, 58(5-6):446-451.
47. Johnston IA. Quantitative analysis of muscle breakdown during starvation in the marine flatfish Pleuronectes platessa. Cell Tissue Res 1981, 214(2):369-386.
48. Montgomery WL, Pollak PE. Gut anatomy and pH in a red sea surgeonfish, canthurus nigrofuscus. Mar Ecol Prog Ser 1988, 44:7-13.
49. Hall KC, Bellwood DR. Histological effects of cyanide, stress and starvation on the intestinal mucosa of Pomacentrus coelestis, a marine aquarium fish species. J Fish Biol 1995, 47(3):438-454.
50. Baumgarner BL, Bharadwaj AS, Inerowicz D, Goodman AS, Brown PB. Proteomic analysis of rainbow trout (Oncorhynchus mykiss) intestinal epithelia: physiological acclimation to short-term starvation. Comp Biochem Physiol Part D Genomics Proteomics 2013, 8(1):58-64. 10.1016/j.cbd.2012.11.001, 23261852.
51. Cham BE. Importance of apolipoproteins in lipid metabolism. Chem Biol Interact 1978, 20(3):263-277. 10.1016/0009-2797(78)90105-9, 207449.
52. Jost R, Berkowitz O, Shaw J, Masle J. Biochemical characterization of two wheat phosphoethanolamine N-methyltransferase isoforms with different sensitivities to inhibition by phosphatidic acid. J Biol Chem 2009, 284:31962-31971. 10.1074/jbc.M109.022657, 2797268, 19762471.
53. Zheng W, Liu G, Ao J, Chen X. Expression analysis of immune-relevant genes in the spleen of large yellow croaker (Pseudosciaena crocea) stimulated with poly I:C. Fish Shellfish Immunol 2006, 21(4):414-430. 10.1016/j.fsi.2006.01.006, 16603383.
54. Nungester WJ, Wolf AA, Jourdonais LF. Effect of gastric mucin on virulence of bacteria in intraperitoneal injections in the mouse. Proc Soc Exp Biol Med 1932, 30(2):120-121.
55. Blum S, Schiffrin EJ. Intestinal microflora and homeostasis of the mucosal immune response: implications for probiotic bacteria?. Curr Issues Intest Microbiol 2003, 4(2):53-60.
56. Dhabhar FS. Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation 2009, 16(5):300-317. 10.1159/000216188, 2790771, 19571591.
57. Hicks RE, Amann RI, Stahl DA. Dual staining of natural bacterioplankton with 4′,6-Diamidino-2-Phenylindole and fluorescent oligonucleotide probes targeting kingdom-level 16 s Ribosomal-Rna sequences. Appl Environ Microb 1992, 58(7):2158-2163.
58. Kane MD, Poulsen LK, Stahl DA. Monitoring the enrichment and isolation of Sulfate-reducing bacteria by using oligonucleotide hybridization probes designed from environmentally derived 16 s ribosomal-Rna sequences. Appl Environ Microb 1993, 59(3):682-686.
59. Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Dore J. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microb 1999, 65(11):4799-4807.
60. Xia JH, Yue GH. Identification and analysis of immune-related transcriptome in Asian seabass Lates calcarifer. BMC Genomics 2010, 11:356. 10.1186/1471-2164-11-356, 2893601, 20525308.
61. Xia JH, He XP, Bai ZY, Lin G, Yue GH. Analysis of the Asian Seabass Transcriptome Based on Expressed Sequence Tags. DNA Res 2011, 18(6):513-522. 10.1093/dnares/dsr036, 3223082, 22086997.
62. Xia JH, Liu P, Liu F, Lin G, Sun F, Tu RJ, Yue GH. Analysis of stress-responsive transcriptome in the intestine of Asian seabass (Lates calcarifer) using RNA-Seq. DNA Res 2013, 20(5):449-460. 10.1093/dnares/dst022, 3789556, 23761194.
63. Peña AA, Bols NC, Marshall SH. An evaluation of potential reference genes for stability of expression in two salmonid cell lines after infection with either Piscirickettsia salmonis or IPNV. BMC Res Notes 2010, 3:101. 10.1186/1756-0500-3-101, 2873344, 20398263.
64. Leelatanawit R, Klanchui A, Uawisetwathana U, Karoonuthaisiri N. Validation of reference genes for real-time PCR of reproductive system in the black tiger shrimp. Plos One 2012, 7(12):e52677. 10.1371/journal.pone.0052677, 3532477, 23285145.
65. Li RQ, Zhu HM, Ruan J, Qian WB, Fang XD, Shi ZB, Li YR, Li ST, Shan G, Kristiansen K, Li SG, Yang HM, Wang J, Wang J. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010, 20(2):265-272. 10.1101/gr.097261.109, 2813482, 20019144.
66. Patel RK, Jain M. NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. Plos One 2012, 7(2):e30619. 10.1371/journal.pone.0030619, 3270013, 22312429.
67. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9(4):357-359. 10.1038/nmeth.1923, 3322381, 22388286.
68. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079. 10.1093/bioinformatics/btp352, 2723002, 19505943.
69. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. The COG database: an updated version includes eukaryotes. BMC Bioinforma 2003, 4:41.
70. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 2007, 73(16):5261-5267.
71. Huson DH, Auch AF, Qi J, Schuster SC. MEGAN analysis of metagenomic data. Genome Res 2007, 17(3):377-386. 10.1101/gr.5969107, 1800929, 17255551.
72. Parks DH, Beiko RG. Identifying biologically relevant differences between metagenomic communities. Bioinformatics 2010, 26(6):715-721. 10.1093/bioinformatics/btq041, 20130030.
73. Logares R, Haverkamp THA, Kumar S, Lanzénd A, Nederbragtc AJ, Quinceg C, Kauserud H. Environmental microbiology through the lens of high-throughput DNA sequencing: Synopsis of current platforms and bioinformatics approaches. J Microbiol Methods 2012, 91:106-113. 10.1016/j.mimet.2012.07.017, 22849829.
74. Dinsdale EA, Pantos O, Smriga S, Edwards RA, Angly F, Wegley L, Hatay M, Hall D, Brown E, Haynes M, Krause L, Sala E, Sandin SA. Microbial ecology of four coral atolls in the northern line islands. Plos One 2008, 3(2):e1584. 10.1371/journal.pone.0001584, 2253183, 18301735.