Abstract
As one of the dominant waterfowl species of wetland areas in the Qinghai-Tibet Plateau, since 2003, artificial rearing of bar-headed geese (Anser indicus) has increased in several provinces of China for the purpose of conservation and economic development. In this study, we systematically characterized the microbial community diversity, compositions and predicted functions of semi-artificially reared bar-headed geese by sampling five different gut locations (the oropharynxs, crops, gizzards, ceca, and cloacae) along the gastrointestinal tracts of three individuals. Alpha diversity analyses showed that the gizzards had the richest species diversity and that the ceca had the least. Beta diversity analyses showed that the cecal samples formed their own cluster, while samples from the oropharynxs, crops, gizzards, and cloacae overlapped with each other. At the phylum level, Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Fusobacteria constituted the top five dominant phyla among all five gastrointestinal sections. At the genus level, a total of 10 genera with proportions above 2.5% were found to be significantly different among the gastrointestinal sections. Furthermore, 53 genera were detected in all gastrointestinal sections of bar-headed geese. PICRUSt data also predicted a group of microbial functions overrepresented in the different segments of the gastrointestinal tracts. Understanding the microbiota along the bar-headed geese gastrointestinal tracts is essential for future microbiological study of this bird and may contribute to the development of geese husbandry.
Similar content being viewed by others
References
Barbosa A, Balagué V, Valera F, Martínez A, Benzal J, Motas M, Diaz JI, Mira A, Pedrós-Alió C (2016) Age-related differences in the gastrointestinal microbiota of chinstrap penguins (Pygoscelis antarctica). PLoS One 11:e0153215. https://doi.org/10.1371/journal.pone.0153215
Bennett DC, Tun HM, Kim JE, Leung FC, Cheng KM (2013) Characterization of cecal microbiota of the emu (Dromaius novaehollandiae). Vet Microbiol 166:304–310. https://doi.org/10.1016/j.vetmic.2013.05.018
Chao A, Bunge J (2002) Estimating the number of species in a stochastic abundance model. Biometrics 58:531–539. https://doi.org/10.1111/j.0006-341X.2002.00531.x
Dominianni C, Sinha R, Goedert JJ, Pei Z, Yang L, Hayes RB, Ahn J (2015) Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One 10:e0124599. https://doi.org/10.1371/journal.pone.0124599
Drovetski SV, O'Mahoney M, Ransome EJ, Matterson KO, Lim HC, Chesser RT, Graves GR (2018) Spatial organization of the gastrointestinal microbiota in urban Canada geese. Sci Rep 8:3713. https://doi.org/10.1038/s41598-018-21892-y
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998. https://doi.org/10.1038/nmeth.2604
Feare CJ, Kato T, Thomas R (2010) Captive rearing and release of bar-headed geese (Anser indicus) in China: a possible HPAI H5N1 virus infection route to wild birds. J Wildl Dis 46:1340–1342. https://doi.org/10.7589/0090-3558-46.4.1340
Garcia-Amado MA, Shin H, Sanz V, Lentino M, Martínez LM, Contreras M, Michelangeli F, Domínguez-Bello MG (2018) Comparison of gizzard and intestinal microbiota of wild neotropical birds. PLoS One 13:e0194857. https://doi.org/10.1371/journal.pone.0194857
Goldstein DL, Skadhauge E (2000) Renal and extrarenal regulation of body fluid composition. In: Whittow GC (ed) Sturkie’s avian physiology, 5th edn. Wiley, New York, pp 265–298
Gong J, Si W, Forster RJ, Huang R, Yu H, Yin Y, Yang C, Han Y (2007) 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts: from crops to ceca. FEMS Microbiol Ecol 59:147–157. https://doi.org/10.1111/j.1574-6941.2006.00193.x
Hadley TL (2005) Disorders of the psittacine gastrointestinal tract. Vet Clin North Am Exot Anim Pract 8:329–349. https://doi.org/10.1016/j.cvex.2005.01.001
Hird SM (2017) Evolutionary biology needs wild microbiomes. Front Microbiol 8:725. https://doi.org/10.3389/fmicb.2017.00725
Hubalek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659. https://doi.org/10.1675/063.035.0314
Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109–D114. https://doi.org/10.1093/nar/gkr988
Kohl KD (2012) Diversity and function of the avian gut microbiota. J Comp Physiol B 182:591–602. https://doi.org/10.1007/s00360-012-0645-z
Kohl KD, Amaya J, Passement CA, Dearing MD, McCue MD (2014) Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts. FEMS Microbiol Ecol 90:883–894. https://doi.org/10.1111/1574-6941.12442
Kohl KD, Connelly JW, Dearing MD, Forbey JS (2016) Microbial detoxification in the gut of a specialist avian herbivore, the greater sage-grouse. FEMS Microbiol Lett 363:fnw144. https://doi.org/10.1093/femsle/fnw144
Kohl KD, Brun A, Caviedes-Vidal E, Karasov WH (2018) Age-related changes in the gut microbiota of wild house sparrow nestlings. Ibis 161:184–191. https://doi.org/10.1111/ibi.12618
Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
Laviad-Shitrit S, Izhaki I, Lalzar M, Halpern M (2019) Comparative analysis of intestine microbiota of four wild waterbird species. Front Microbiol 10:1911. https://doi.org/10.3389/fmicb.2019.01911
Lee FJ, Rusch DB, Stewart FJ, Mattila HR, Newton IL (2015) Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ Microbiol 17:796–815. https://doi.org/10.1111/1462-2920.12526
Lee WY (2015) Avian gut microbiota and behavioral studies. Kor J Orni 22:1–11
Lu Y, Rock CO (2010) Transcriptional regulation of fatty acid biosynthesis in Streptococcus pneumoniae. Mol Microbiol 59:551–566. https://doi.org/10.1111/j.1365-2958.2005.04951.x
Matsui H, Kato Y, Chikaraishi T, Moritani M, Ban-Tokuda T, Wakita M (2010) Microbial diversity in ostrich ceca as revealed by 16S ribosomal RNA gene clone library and detection of novel Fibrobacter species. Anaerobe 16:83–93. https://doi.org/10.1016/j.anaerobe.2009.07.005
Moon CD, Young W, Maclean PH, Cookson AL, Bermingham EN (2018) Metagenomic insights into the roles of Proteobacteria in the gastrointestinal microbiomes of healthy dogs and cats. Microbiologyopen 7:e00677. https://doi.org/10.1002/mbo3.677
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
Roggenbuck M, Bærholm Schnell I, Blom N, Bælum J, Bertelsen MF, Sicheritz-Pontén T, Sørensen SJ, Gilbert MT, Graves GR, Hansen LH (2014) The microbiome of New World vultures. Nat Commun 5:5498. https://doi.org/10.1038/ncomms9774
Roto SM, Rubinelli PM, Ricke SC (2015) An introduction to the avian gut microbiota and the effects of yeast-based prebiotic-type compounds as potential feed additives. Front Vet Sci 2:28. https://doi.org/10.3389/fvets.2015.00028
Ruiz-Rodriguez M, Valdivia E, Soler JJ, Martín-Vivaldi M, Martín-Platero AM, Martínez-Bueno M (2009) Symbiotic bacteria living in the hoopoe's uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626. https://doi.org/10.1242/jeb.031336
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Shannon CE (1997) The mathematical theory of communication. MD Comput 14:306–317
Shin NR, Whon TW, Bae JW (2015) Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol 33:496–503. https://doi.org/10.1016/j.tibtech.2015.06.011
Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427. https://doi.org/10.1655/HERPETOLOGICA-D-13-00061
Takekawa JY, Heath SR, Douglas DC, Perry WM, Javed S, Newman SH, Suwal RN, Rahmani AR, Choudhury BC, Prosser DJ, Yan BP, Hou YS, Batbayar N, Natsagdorj T, Bishop CM, Butler PJ, Frappell PB, Milsom WK, Scott GR, Hawkes LA, Wikelski M (2009) Geographic variation in bar-headed geese Anser indicus: connectivity of wintering areas and breeding grounds across a broad front. Wildfowl 59:100–123
Thomas F, Hehemann JH, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut bacteroidetes: the food connection. Front Microbiol 2:93. https://doi.org/10.3389/fmicb.2011.00093
Videvall E, Strandh M, Engelbrecht A, Cloete S, Cornwallis CK (2018) Measuring the gut microbiome in birds: Comparison of faecal and cloacal sampling. Mol Ecol Resour 18:424–434. https://doi.org/10.1111/1755-0998.12744
Waite DW, Eason DK, Taylor MW (2014) Influence of hand rearing and bird age on the fecal microbiota of the critically endangered kakapo. Appl Environ Microbiol 80:4650–4658. https://doi.org/10.1128/AEM.00975-14
Waite DW, Taylor MW (2014) Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol 5:223. https://doi.org/10.3389/fmicb.2014.00223
Waite DW, Taylor MW (2015) Exploring the avian gut microbiota: current trends and future directions. Front Microbiol 6:673. https://doi.org/10.3389/fmicb.2015.00673
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07
Wang W, Cao J, Li JR, Yang F, Li Z, Li LX (2016a) Comparative analysis of the gastrointestinal microbial communities of bar-headed goose (Anser indicus) in different breeding patterns by high-throughput sequencing. Microbiol Res 182:59–67. https://doi.org/10.1016/j.micres.2015.10.003
Wang W, Cao J, Yang F, Wang X, Zheng S, Sharshov K, Li L (2016b) High-throughput sequencing reveals the core gut microbiome of bar-headed goose (Anser indicus) in different wintering areas in Tibet. Microbiologyopen 5:287–295. https://doi.org/10.1002/mbo3.327
Wang W, Zheng S, Sharshov K, Cao J, Sun H, Yang F, Wang X, Li L (2016c) Distinctive gut microbial community structure in both the wild and farmed Swan goose (Anser cygnoides). J Basic Microbiol 56:1299–1307. https://doi.org/10.1002/jobm.201600155
Wang W, Wang AZ, Yang YS, Wang F, Liu YB, Zhang YH, Sharshov K, Gui LS (2019) Composition, diversity and function of gastrointestinal microbiota in wild red-billed choughs (pyrrhocorax pyrrhocorax). Int Microbiol. 22:491–500. https://doi.org/10.1007/s10123-019-00076-2
Wilkinson TJ, Cowan AA, Vallin HE, Onime LA, Oyama LB, Cameron SJ, Gonot C, Moorby JM, Waddams K, Theobald VJ, Leemans D, Bowra S, Nixey C, Huws SA (2017) Characterization of the microbiome along the gastrointestinal tract of growing Turkeys. Front Microbiol 8:1089. https://doi.org/10.3389/fmicb.2017.01089
Yang H, Xiao Y, Gui G, Li J, Wang J, Li D (2018) Microbial community and short-chain fatty acid profile in gastrointestinal tract of goose. Poult Sci 97:1420–1428. https://doi.org/10.3382/ps/pex438
Zhao N, Wang S, Li H, Liu S, Li M, Luo J, Su W, He H (2018) Influence of novel highly pathogenic avian influenza A (H5N1) virus infection on migrating whooper swans fecal microbiota. Front Cell Infect Microbiol 8:46. https://doi.org/10.3389/fcimb.2018.00046
Acknowledgments
We thank the Fei Yan specialized breeding and rearing farming cooperative for permission to undertake this study on their property. The authors would like to express their sincere thanks to the editor in chief, editor, and anonymous reviewers for their valuable suggestions in revising the manuscript.
Funding
The study was supported by the Natural Science Foundation of Qinghai Province of China (Grant No. 2018-ZJ-932Q), the National Natural Science Foundation of China (Grant No. 31460569 and 31960277), the Project of Qinghai Science & Technology Department (Grant No. 2016-ZJ-Y01), the Open Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (Grant No. 2017-ZZ-21) and the project of Tao He Yuan National Wetland Park in Qinghai Province (Grant No. 2018-THY-01). Dr. Wen Wang was supported by “1000 Talent” programs of Qinghai Province.
Author information
Authors and Affiliations
Contributions
Wen Wang conceived and designed the study. Zhuoma Lancuo and Shuoying Wang collected the samples. Fang Wang, Aizhen Wang and Kirill Sharshov performed the data analysis. Wen Wang wrote the first draft. Kirill Sharshov and Alexey Druzyaka discussed and revised the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
All experiments involving animals were reviewed and approved by the Ethical Committee of Qinghai University and conformed to the guidelines for the care and use of experimental animals established by the Ministry of Science and Technology of the People’s Republic of China (Publication no. 2006-398).
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 541 kb)
Rights and permissions
About this article
Cite this article
Wang, W., Wang, F., Wang, A. et al. Characterization of the microbiome along the gastrointestinal tracts of semi-artificially reared bar-headed geese (Anser indicus). Folia Microbiol 65, 533–543 (2020). https://doi.org/10.1007/s12223-019-00758-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-019-00758-4