Convergence of gut microbiotas in the adaptive radiations of African cichlid fishes
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
201067
European Research Council - International
PubMed
28509910
PubMed Central
PMC5560477
DOI
10.1038/ismej.2017.62
PII: ismej201762
Knihovny.cz E-zdroje
- MeSH
- Bacteria klasifikace genetika izolace a purifikace MeSH
- cichlidy mikrobiologie fyziologie MeSH
- ekologie MeSH
- fylogeneze MeSH
- fyziologická adaptace MeSH
- fyziologie bakterií účinky záření MeSH
- genetická variace účinky záření MeSH
- jezera mikrobiologie MeSH
- sluneční záření MeSH
- stravovací zvyklosti účinky záření MeSH
- střevní mikroflóra * účinky záření MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Ecoevolutionary dynamics of the gut microbiota at the macroscale level, that is, in across-species comparisons, are largely driven by ecological variables and host genotype. The repeated explosive radiations of African cichlid fishes in distinct lakes, following a dietary diversification in a context of reduced genetic diversity, provide a natural setup to explore convergence, divergence and repeatability in patterns of microbiota dynamics as a function of the host diet, phylogeny and environment. Here we characterized by 16S rRNA amplicon sequencing the gut microbiota of 29 cichlid species from two distinct lakes/radiations (Tanganyika and Barombi Mbo) and across a broad dietary and phylogenetic range. Within each lake, a significant deviation between a carnivorous and herbivorous lifestyle was found. Herbivore species were characterized by an increased bacterial taxonomic and functional diversity and converged in key compositional and functional community aspects. Despite a significant lake effect on the microbiota structure, this process has occurred with remarkable parallels in the two lakes. A metabolic signature most likely explains this trend, as indicated by a significant enrichment in herbivores/omnivores of bacterial taxa and functions associated with fiber degradation and detoxification of plant chemical compounds. Overall, compositional and functional aspects of the gut microbiota individually and altogether validate and predict main cichlid dietary habits, suggesting a fundamental role of gut bacteria in cichlid niche expansion and adaptation.
Department of Zoology Charles University Prague Prague Czech Republic
Faculty of Science University of Ngaoundere Ngaoundere Cameroon
Zobrazit více v PubMed
Adams DC. (2014). A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst Biol 63: 685–697. PubMed
Afgan E, Baker D, van den Beek M, Blankenberg D, Bouvier D, Cech M et al. (2016). The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2016 update. Nucleic Acids Res 44: W3–W10. PubMed PMC
Ayayee PA, Larsen T, Rosa C, Felton GW, Ferry JG, Hoover K. (2016). Essential amino acid supplementation by gut microbes of a wood-feeding cerambycid. Environ Entomol 45: 66–73. PubMed PMC
Baldo L, Riera JL, Tooming-Klunderud A, Alba MM, Salzburger W. (2015). Gut microbiota dynamics during dietary shift in Eastern African cichlid fishes. PLoS One 10: e0127462. PubMed PMC
Baothman OA, Zamzami MA, Taher I, Abubaker J, Abu-Farha M. (2016). The role of gut microbiota in the development of obesity and diabetes. Lipids Health Dis 15: 108. PubMed PMC
Blomberg SP, Garland Jr T, Ives AR. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57: 717–745. PubMed
Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Knight R, Caporaso JG et al. (2014). Individuals' diet diversity influences gut microbial diversity in two freshwater fish (threespine stickleback and Eurasian perch). Ecol Lett 17: 979–987. PubMed PMC
Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S et al. (2014). The genomic substrate for adaptive radiation in African cichlid fish. Nature 513: 375–381. PubMed PMC
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336. PubMed PMC
Cayrou C, Sambe B, Armougom F, Raoult D, Drancourt M. (2013). Molecular diversity of the Planctomycetes in the human gut microbiota in France and Senegal. Acta Pathol Microbiol Immunol Scand 121: 1082–1090. PubMed
Clark DP, Dunlap P, Madigan M, Martinko J. (2009) Brock Biology of Microorganisms. Scientific Publisher: Beijing, China.
Clements KD, Angert ER, Montgomery WL, Choat JH. (2014). Intestinal microbiota in fishes: what's known and what's not. Mol Ecol 23: 1891–1898. PubMed
Costello EK, Stagaman K, Dethlefsen L, Bohannan BJ, Relman DA. (2012). The application of ecological theory toward an understanding of the human microbiome. Science 336: 1255–1262. PubMed PMC
Davis AM, Unmack PJ, Pusey BJ, Pearson RG, Morgan DL. (2013). Ontogenetic development of intestinal length and relationships to diet in an Australasian fish family (Terapontidae). BMC Evol Biol 13: 53. PubMed PMC
Day JJ, Cotton JA, Barraclough TG. (2008). Tempo and mode of diversification of lake Tanganyika cichlid fishes. PLoS One 3: e1730. PubMed PMC
De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S et al. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107: 14691–14696. PubMed PMC
Delsuc F, Metcalf JL, Wegener Parfrey L, Song SJ, Gonzalez A, Knight R. (2014). Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol 23: 1301–1317. PubMed
Edward Stevens C, Hume ID. (2004) Comparative Physiology of the Vertebrate Digestive System. 2nd edn. Cambridge University Press: Cambridge, New York, NY, USA.
Flint HJ, Scott KP, Duncan SH, Louis P, Forano E. (2012). Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3: 289–306. PubMed PMC
Frey JC, Rothman JM, Pell AN, Nizeyi JB, Cranfield MR, Angert ER. (2006). Fecal bacterial diversity in a wild gorilla. Appl Environ Microbiol 72: 3788–3792. PubMed PMC
Garcia-Amado MA, Godoy-Vitorino F, Piceno YM, Tom LM, Andersen GL, Herrera EA et al. (2012). Bacterial diversity in the cecum of the world's largest living rodent (Hydrochoerus hydrochaeris. Microb Ecol 63: 719–725. PubMed
Genner MJ, Seehausen O, Lunt DH, Joyce DA, Shaw PW, Carvalho GR et al. (2007). Age of cichlids: new dates for ancient lake fish radiations. Mol Biol Evol 24: 1269–1282. PubMed
Giatsis C, Sipkema D, Smidt H, Heilig H, Benvenuti G, Verreth J et al. (2015). The impact of rearing environment on the development of gut microbiota in tilapia larvae. Scientific Rep 5: 18206. PubMed PMC
Graham D, Kim H, Lindner A. (2002) Methanotrophic bacteria. In: Bitton G (ed). Encyclopedia of Environmental Microbiology. Wiley: New York, NY, USA, pp 1923–1936.
Hammer TJ, Bowers MD. (2015). Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179: 1–14. PubMed
Hansen AK, Moran NA. (2014). The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol 23: 1473–1496. PubMed
Hata H, Tanabe AS, Yamamoto S, Toju H, Kohda M, Hori M. (2014). Diet disparity among sympatric herbivorous cichlids in the same ecomorphs in Lake Tanganyika: amplicon pyrosequences on algal farms and stomach contents. BMC Biol 12: 90. PubMed PMC
Hata H, Shibata J, Omori K, Kohda M, Hori M. (2015). Depth segregation and diet disparity revealed by stable isotope analyses in sympatric herbivorous cichlids in Lake Tanganyika. Zool Lett 1: 15. PubMed PMC
Hird SM, Sanchez C, Carstens BC, Brumfield RT. (2015). Comparative gut microbiota of 59 neotropical bird species. Front Microbiol 6: 1403. PubMed PMC
Jost L. (2006). Entropy and diversity. Oikos 113: 363–375.
Karasov WH, Martinez del Rio C. (2007) Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins. Princeton University Press: Princeton, NJ, USA.
Karasov WH, Martinez del Rio C, Caviedes-Vidal E. (2011). Ecological physiology of diet and digestive systems. Annu Rev Physiol 73: 69–93. PubMed
Kohl KD, Dearing MD. (2012). Experience matters: prior exposure to plant toxins enhances diversity of gut microbes in herbivores. Ecol Lett 15: 1008–1015. PubMed
Kohl KD, Brun A, Magallanes M, Brinkerhoff J, Laspiur A, Acosta JC et al. (2016. a). Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard. J Exp Biol 219: 1903–1912. PubMed
Kohl KD, Connelly JW, Dearing MD, Forbey JS. (2016. b). Microbial detoxification in the gut of a specialist avian herbivore, the Greater Sage-Grouse. FEMS Microbiol Lett 363: fnw144. PubMed
Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD. (2014). Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett 17: 1238–1246. PubMed
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA et al. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31: 814–821. PubMed PMC
Larsen T, Ventura M, Maraldo K, Triado-Margarit X, Casamayor EO, Wang YV et al. (2016). The dominant detritus-feeding invertebrate in arctic peat soils derives its essential amino acids from gut symbionts. J Anim Ecol 85: 1275–1285. PubMed
Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. (2008). Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6: 776–788. PubMed PMC
Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F et al. (2016). The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Scientific Rep 6: 24340. PubMed PMC
Matschiner M, Musilova Z, Barth JM, Starostova Z, Salzburger W, Steel M et al. (2017). Bayesian phylogenetic estimation of clade ages supports Trans-Atlantic dispersal of cichlid fishes. Syst Biol 66: 3–22. PubMed
Meyer BS, Matschiner M, Salzburger W. (2014). A tribal level phylogeny of Lake Tanganyika cichlid fishes based on a genomic multi-marker approach. Mol Phylogenet Evol 83C: 56–71. PubMed PMC
Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L et al. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332: 970–974. PubMed PMC
Muschick M, Indermaur A, Salzburger W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Curr Biol 22: 2362–2368. PubMed
Muschick M, Nosil P, Roesti M, Dittmann MT, Harmon L, Salzburger W. (2014). Testing the stages model in the adaptive radiation of cichlid fishes in East African Lake Tanganyika. Proc Biol Sci/R Soc 281: 20140605. PubMed PMC
Nelson KE, Zinder SH, Hance I, Burr P, Odongo D, Wasawo D et al. (2003). Phylogenetic analysis of the microbial populations in the wild herbivore gastrointestinal tract: insights into an unexplored niche. Environ Microbiol 5: 1212–1220. PubMed
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB et al. (2015). vegan: Community Ecology Package. R package version 2.3-0. Available at: http://CRAN.R-project.org/package=vegan.
Pennisi E. (2017). How do gut microbes help herbivores? Counting the ways. Science 355: 236–236. PubMed
Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL et al. (2013). Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341: 1241214. PubMed PMC
Russell JA, Moreau CS, Goldman-Huertas B, Fujiwara M, Lohman DJ, Pierce NE. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc Natl Acad Sci USA 106: 21236–21241. PubMed PMC
Salzburger W. (2009). The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18: 169–185. PubMed
Sanders JG, Beichman AC, Roman J, Scott JJ, Emerson D, McCarthy JJ et al. (2015). Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat Commun 6: 8285. PubMed PMC
Schliewen UK, Tautz D, Paabo S. (1994). Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368: 629–632. PubMed
Schnorr SL, Candela M, Rampelli S, Centanni M, Consolandi C, Basaglia G et al. (2014). Gut microbiome of the Hadza hunter-gatherers. Nat Commun 5: 3654. PubMed PMC
Sonnenburg JL, Backhed F. (2016). Diet–microbiota interactions as moderators of human metabolism. Nature 535: 56–64. PubMed PMC
Soverini M, Quercia S, Biancani B, Furlati S, Turroni S, Biagi E et al. (2016). The bottlenose dolphin (Tursiops truncatus faecal microbiota. FEMS Microbiol Ecol 92: fiw055. PubMed
Spor A, Koren O, Ley R. (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9: 279–290. PubMed
Sturmbauer C, Mark W, Dallinger R. (1992). Ecophysiology of Aufwuchs-eating cichlids in Lake Tanganyika: niche separation by trophic specialization. Environ Biol Fishes 35: 1573–5133.
Sullam KE, Essinger SD, Lozupone CA, O'Connor MP, Rosen GL, Knight R et al. (2012). Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol 21: 3363–3378. PubMed PMC
Trewavas E, Green J, Corbe SA. (1972). Ecological studies on crater lakes in West Cameroon Fishes of Barombi Mbo. J Zool 167: 41–95.
Wagner CE, McIntyre PB, Buels KS, Gilbert DM, Michel E. (2009). Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct Ecol 23: 1122–1131.
Wertz JT, Kim E, Breznak JA, Schmidt TM, Rodrigues JL. (2012). Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Appl Environ Microbiol 78: 1544–1555. PubMed PMC
Xue Z, Zhang W, Wang L, Hou R, Zhang M, Fei L et al. (2015). The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. MBio 6: e00022–00015. PubMed PMC
Zhou XX, Pan YJ, Wang YB, Li WF. (2007). In vitro assessment of gastrointestinal viability of two photosynthetic bacteria, Rhodopseudomonas palustris and Rhodobacter sphaeroides. J Zhejiang Univ Sci B 8: 686–692. PubMed PMC