Comparative Analyses of the Digestive Tract Microbiota of New Guinean Passerine Birds

. 2018 ; 9 () : 1830. [epub] 20180810

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30147680

The digestive tract microbiota (DTM) plays a plethora of functions that enable hosts to exploit novel niches. However, our understanding of the DTM of birds, particularly passerines, and the turnover of microbial communities along the digestive tract are limited. To better understand how passerine DTMs are assembled, and how the composition changes along the digestive tract, we investigated the DTM of seven different compartments along the digestive tract of nine New Guinean passerine bird species using Illumina MiSeq sequencing of the V4 region of the 16S rRNA. Overall, passerine DTMs were dominated by the phyla Firmicutes and Proteobacteria. We found bird species-specific DTM assemblages and the DTM of different compartments from the same species tended to cluster together. We also found a notable relationship between gut community similarity and feeding guilds (insectivores vs. omnivores). The dominant bacterial genera tended to differ between insectivores and omnivores, with insectivores mainly having lactic acid bacteria that may contribute to the breakdown of carbohydrates. Omnivorous DTMs were more diverse than insectivores and dominated by the bacterial phyla Proteobacteria and Tenericutes. These bacteria may contribute to nitrogen metabolism, and the diverse omnivorous DTMs may allow for more flexibility with varying food availability as these species have wider feeding niches. In well-sampled omnivorous species, the dominant bacterial genera changed along the digestive tracts, which was less prominent for insectivores. In conclusion, the DTMs of New Guinean passerines seem to be species specific and, at least in part, be shaped by bird diet. The sampling of DTM along the digestive tract improved capturing of a more complete set of members, with implications for our understanding of the interactions between symbiont and gut compartment functions.

Zobrazit více v PubMed

Benskin C. M. H., Wilson K., Jones K., Hartley I. R. (2009). Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol. Rev. 84, 349–373. 10.1111/j.1469-185X.2008.00076.x PubMed DOI

Cafaro M. J., Poulsen M., Little A. E. F., Price S. L., Gerardo N. M., Wong B., et al. (2011). Specificity in the symbiotic association between fungus-growing ants and protective PubMed DOI PMC

Ceja-Navarro J. A., Vega F. A., Karaoz U., Hao Z., Jenkins S., Lim H. C., et al. (2015). Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6:7618. 10.1038/ncomms8618 PubMed DOI PMC

Dewar M. L., Arnold J. P. Y., Dann P., Trathan P., Groscolas R., Smith S. (2013). Interspecific variations in the gastrointestinal microbiota in penguins. Microbiologyopen 2, 195–204. 10.1002/mbo3.66 PubMed DOI PMC

Dickinson E. C., Christidis L. (eds). (2014). The Howard and Moore Complete Checklist of the Birds of the World, Vol. 2:

Dietrich C., Köhler T., Brune A. (2014). The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl. Environ. Microbiol. 80, 2261–2269. 10.1128/AEM.04206-13 PubMed DOI PMC

Drovetski S. V., O'Mahony M., Ransome E. J., Matterson K. O., Lim H. C., Chesser R. T., et al. (2018). Spatial organization of the gastrointestinal microbiota in urban Canada geese. Sci. Rep. 8:3713 10.1038/s41598-018-21892-y PubMed DOI PMC

Dumbacher J. P., Deiner K., Thompson L., Fleischer R. C. (2008). Phylogeny of the avian genus Pitohui and the evolution of toxicity in bird. Mol. Phylogenet. Evol. 49, 774–781. 10.1016/j.ympev PubMed DOI

Dumbacher J. P., Spande T. F., Daly J. W. (2000). Batrachotoxin alkaloids from passerine birds: a second toxic bird genus ( PubMed DOI PMC

García-Amado M. A., Shin H., Sanz V., Lentino M., Martínez L. M., Contreras M., et al. (2018). Comparison of gizzard and intestinal microbiota of wild neotropical birds. PLoS ONE 13:e0194857. 10.1371/journal.pone.0194857 PubMed DOI PMC

Glass J. I., Lefkowitz E. J., Glass J. S., Heiner C. R., Chen E. Y., Cassell G. H. (2000). The complete sequence of the mucosal pathogen PubMed DOI

Godoy-Vitorino F., Goldfarb K. C., Karaoz U., Leal S., Garcia-Amado M. A., Hugenholtz P., et al. (2012). Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows. ISME J. 6, 531–541. 10.1038/ismej.2011.131 PubMed DOI PMC

Hammes W. P., Hertel C. (2006). The genera of

Hird S. M. (2017). Evolutionary biology needs wild microbiomes. Front. Microbiol. 8:725. 10.3389/fmicb.2017.00725 PubMed DOI PMC

Hird S. M., Carstens B. C., Cardiff S. W., Dittmann D. L., Brumfield R. B. (2014). Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird ( PubMed DOI PMC

Hird S. M., Sánchez C., Carstens B. C., Brumfield R. T. (2015). Comparative gut microbiota of 59 neotropical bird species. Front. Microbiol. 6:1403. 10.3389/fmicb.2015.01403 PubMed DOI PMC

Huttenhower C., The human microbiome project consortium (2012). Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214. 10.1038/nature11234 PubMed DOI PMC

Kohl K. D. (2012). Diversity and the function of the avian gut microbiota. J. Comp. Physiol. B 182, 591–602. 10.1007/s00360-012-0645-z PubMed DOI

Kohl K. D., Dearing M. D., Bordenstein S. R. (2018). Microbial communities exhibit host species distinguishability and phylosymbiosis along the length of the gastrointestinal tract. Mol. Ecol. 27, 1874–1883. 10.1111/mec.14460 PubMed DOI PMC

Kozich J. J., Westcott S. L., Baxter N. T., Highlander S. K., Schloss P. D. (2013). Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79, 5112–5120. 10.1128/AEM.01043-13 PubMed DOI PMC

Kropáčková L., Tesicky M., Albrecht T., Kubovčiak J., Cisková D., Tomásek O., et al. (2017). Codiversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. Mol. Ecol. 26, 5292–5304. 10.1111/mec.14144 PubMed DOI

LeBlanc D. J. (2006). Enterococcus, in “The Prokaryotes: A Handbook on the Biology of Bacteria,” eds Dworkin M., Falkow S., Rosenberg E., Schleifer K., Stackebrandt E. (New York, NY: Springer Science; ), 175–204.

Lee W. Y. (2015). Avian gut microbiota and behavioral studies. Korean J. Ornithol. 22, 1–11. Available online at: https://www.researchgate.net/profile/Won_Young_Lee2/publication/281350575_Avian_gut_microbiota_and_behavioral_studies/links/55e3ac1908aede0b5733cae4/Avian-gut-microbiota-and-behavioral-studies.pdf

Lewis W. B., Moore F. R., Wang S. (2016). Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico. J. Avian Biol. 47, 659–668. 10.1111/jav.00954 DOI

Ley R. E., Hamady M., Lozupone C., Turnbaugh P. J., Ramey R. R., Bircher J. S., et al. (2008). Evolution of mammals and their gut microbes. Science 320, 1647–1651. 10.1126/science.1155725 PubMed DOI PMC

Lu J., Domingo J. S. (2008). Turkey fecal microbial community structure and functional gene diversity revealed by 16S rRNA and metagenomic sequencing. J. Microbiol. 46, 469–477. 10.1007/s12275-008-0117-z PubMed DOI

Macke E., Tasiemski A., Massol F., Callens M., Decaestecker E. (2017). Life history and the eco-evolutionary dynamics of the gut microbiota. Oikos 126, 508–531. 10.1111/oik.03900 DOI

Muegge B. D., Kuczynski J., Knights D., Clemente J. C., González A., Fontana L., et al. (2011). Diet drives convergence in microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974. 10.1126/science.1198719 PubMed DOI PMC

Otani S., Hansen L. H., Sørensen S. J., Poulsen M. (2016). Bacterial communities in termite fungus combs are comprised of consistent gut deposits and contributions from the environment. Microb. Ecol. 71, 207–220. 10.1007/s00248-015-0692-6 PubMed DOI PMC

Panina E. M., Vistreschak A. G., Mironov A. A., Gelfand M. S. (2001). Regulation of aromatic amino acid biosynthesis in Gamma-Proteobacteria. J. Mol. Microbiol. Biotechnol. 3, 529–543. PubMed

Pikuta E. V. (2014). Section 2: Family Carnobacteraceae in The Lactic Acid Bacteria: Biodiversity and Taxonomy, 1st edn, eds Holzapfel W. H., Wood B. J. B. (Hoboken, NJ: John Wiley & Sons, Ltd; ), 107–108.

Poulsen M., Hu H., Li C., Chen Z., Xu L., Otani S., et al. (2014). Complementary symbiont contributions to plant decomposition in a fungus-farming termite. Proc. Natl. Acad. Sci. U.S.A. 111, 14500–14505. 10.1073/pnas.1319718111 PubMed DOI PMC

Pratt K. T., Beehler B. M. (2015). Birds of New Guinea, 2nd Edn. Princeton, NJ: Princeton University Press.

Preest M. R., Folk G. D., Beuchat C. A. (2003). Decomposition of nitrogenous compounds by intestinal bacteria in hummingbirds. Auk 120, 1091–1101. 10.2307/4090280 DOI

Pukall R., Lipidus A., Rio T. G. D., Copeland A., Tice H., Cheng J., et al. (2010). Complete genome sequence of PubMed DOI PMC

R Core Team (2013). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; Available online at: http://www.R-project.org/

Roggenbuck M., Schnell I. B., Blom N., Bælum J., Bertelsen F. M., Sicheritz-Ponten T., et al. (2014). The microbiome of new world vultures. Nat. Commun. 5:5498. 10.1038/ncomms6498 PubMed DOI

Round J. L., Mazmanian S. K. (2009). The Gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323. 10.1038/nri2515 PubMed DOI PMC

Russell J. A., Moreau C. S., Goldman-Huertas B., Fujiwara M., Lohman D. J., Pierce N. E. (2009). Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Natl. Acad. Sci. U.S.A. 106, 21236–21241. 10.1073/pnas.0907926106 PubMed DOI PMC

Sam K., Koane B., Jeppy S., Sykorova J., Novotny V. (2017). Diet of land birds along an elevational gradient in Papua New Guinea. Sci. Rep. 7:44018. 10.1038/srep44018 PubMed DOI PMC

Sekelja M., Rud I., Knutsen S. H., Denstadli V., Westereng B., Næs T., et al. (2012). Abrupt temporal fluctuations in the chicken fecal microbiota are explained by its gastrointestinal origin. Appl. Environ. Microbiol. 78, 2941–2948. 10.1128/aem.05391-11 PubMed DOI PMC

Sommer F., Bäckhed F. (2013). The gut microbiota - masters of host development and physiology. Nat. Rev. Microbiol. 11, 227–238. 10.1038/nrmicro2974 PubMed DOI

Stanley D., Geier M. S., Chen H., Hughes R. J., Moore R. J. (2015). Comparison of fecal and cecal microbiotas reveals qualitative similarities but quantitative differences. BMC Microbiol. 15:51. 10.1186/s12866-015-0388-6 PubMed DOI PMC

Stevens C. E., and I. D., Hume (1995). Comparative Physiology of the Vertebrate Digestive System, 2 Edn. Cambridge: Cambridge university press.

Svihus B. (2014). Function of the digestive system. J. Appl. Poult. Res. 23, 306–314. 10.3382/japr.2014-00937 DOI

Teyssier A., Rouffaer L. O., Hudin N. S., Strubbe D., Matthysen E., Lens L., et al. (2018). Inside the guts of the city: urban-induced alterations of the gut microbiota in a wild passerine. Sci. Total Environ. 612, 1276–1286. 10.1016/j.scitotenv.2017.09.035 PubMed DOI

Veinberg S., McClay K., Masuda H., Root D., Condee C., Zylstra D. J., et al. (2006). Biodegradation of ether pollutants by PubMed DOI PMC

Vela A. I., Casas-Diaz E., Fernandez-Garayzabal J. F., Serrano E., Agusti S., Porrero M. C., et al. (2015). Estimation of cultivable bacterial diversity in the cloacae and pharynx in eurasian griffon vultures ( PubMed DOI

Videvall E., Strandh M., Engelbrecht A., Cloete S., Cornwallis C. K. (2017). Measuring the gut microbiome in birds: comparison of faecal and cloacal sampling. Mol. Ecol. Resour. 18, 424–434. 10.1111/1755-0998.12744 PubMed DOI

Waite D. W., Taylor M. W. (2015). Exploring the avian gut microbiota: current trends and future directions. Front. Microbiol. 6:673. 10.3389/fmicb.2015.00673 PubMed DOI PMC

Wang W., Cao J., Li J. R., Yang F., Li Z., Li L. X. (2016). Comparative analysis of the gastrointestinal microbial communities of bar-headed goose ( PubMed DOI

White J., Mirleau P., Danchin E., Mulard H., Hatch S. A., Heeb P., et al. (2010). Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol. Lett. 13, 1515–1524. 10.1111/j.1461-0248.2010.01542.x PubMed DOI PMC

Zehr J. P., Jenkins B. D., Short S. M., Steward G. F. (2003). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5, 539–554. 10.1046/j.1462-2920.2003.00451.x PubMed DOI

Zhang Y., Simon S. E., Johnson J. A., Allen M. S. (2017). Spatial microbial composition along the gastrointestinal tract of captive attwater's prairie chicken. Microb. Ecol. 73, 966–977. 10.1007/s00248-016-0870-1 PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Bacterial communities along parrot digestive and respiratory tracts: the effects of sample type, species and time

. 2024 Feb ; 27 (1) : 127-142. [epub] 20230524

Gut microbiota variation between climatic zones and due to migration strategy in passerine birds

. 2023 ; 14 () : 1080017. [epub] 20230201

Variation in diet composition and its relation to gut microbiota in a passerine bird

. 2022 Mar 08 ; 12 (1) : 3787. [epub] 20220308

Specific gut bacterial responses to natural diets of tropical birds

. 2022 Jan 13 ; 12 (1) : 713. [epub] 20220113

Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications

. 2021 Apr 28 ; 288 (1949) : 20210446. [epub] 20210421

Gut microbiota in two recently diverged passerine species: evaluating the effects of species identity, habitat use and geographic distance

. 2021 Mar 10 ; 21 (1) : 41. [epub] 20210310

Flexibility and resilience of great tit (Parus major) gut microbiomes to changing diets

. 2021 Feb 18 ; 3 (1) : 20. [epub] 20210218

Great Tit (Parus major) Uropygial Gland Microbiomes and Their Potential Defensive Roles

. 2020 ; 11 () : 1735. [epub] 20200728

Cloacal swabs and alcohol bird specimens are good proxies for compositional analyses of gut microbial communities of Great tits (Parus major)

. 2020 Mar 17 ; 2 (1) : 9. [epub] 20200317

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...