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Background

Gut microbiota play crucial roles in host health. Wild birds and domestic poultry often occupy sympatric habitats, which facilitate the mutual transmission of intestinal microbes. However, the distinct intestinal microbial communities between sympatric wild birds and poultry remain unknown. At present, the risk of interspecies transmission of pathogenic bacteria between wild and domestic host birds is also a research hotspot.

Methods

This study compared the intestinal bacterial communities of the overwintering Hooded Crane (Grus monacha) and the Domestic Goose (Anser anser domesticus) at Shengjin Lake, China, using Illumina high-throughput sequencing technology (Mi-Seq platform).

Results

Our results revealed that Firmicutes, Actinobacteria, Proteobacteria, Bacteroidetes and Chloroflexi were the dominant bacterial phyla in both hosts. The gut bacterial community composition differed significantly between sympatric Hooded Cranes and Domestic Geese. However, the hosts exhibited little variation in gut bacterial alpha-diversity. The relative abundance of Firmicutes was significantly higher in the guts of the Hooded Cranes, while the relative abundances of Actinobacteria, Proteobacteria, Bacteroidete and Chloroflexi were significantly higher in guts of Domestic Geese. Moreover, a total of 132 potential pathogenic operational taxonomic units (OTUs) were detected in guts of Hooded Cranes and Domestic Geese, and 13 pathogenic OTUs (9.8%) were found in both host guts. Pathogenic bacterial community composition and diversity differed significantly between hosts.

Conclusions

The results showed that the gut bacterial community composition differs significantly between sympatric Hooded Cranes and Domestic Geese. In addition, potential pathogens were detected in the guts of both Hooded Cranes and Domestic Geese, with 13 pathogenic OTUs overlapping between the two hosts, suggesting that more attention should be paid to wild birds and poultry that might increase the risk of disease transmission in conspecifics and other mixed species.


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Comparing the intestinal bacterial communies of sympatric wintering Hooded Crane (Grus monacha) and Domestic Goose (Anser anser domesticus)

Show Author's information Rong Fu1,2Xingjia Xiang1,2Yuanqiu Dong1,2Lei Cheng1,2Lizhi Zhou1,2( )
School of Resources and Environmental Engineering, Anhui University, Hefei 230601, China
Anhui Province Key Laboratory of Wetland Ecological Protection and Restoration (Anhui University), Hefei 230601, China

Abstract

Background

Gut microbiota play crucial roles in host health. Wild birds and domestic poultry often occupy sympatric habitats, which facilitate the mutual transmission of intestinal microbes. However, the distinct intestinal microbial communities between sympatric wild birds and poultry remain unknown. At present, the risk of interspecies transmission of pathogenic bacteria between wild and domestic host birds is also a research hotspot.

Methods

This study compared the intestinal bacterial communities of the overwintering Hooded Crane (Grus monacha) and the Domestic Goose (Anser anser domesticus) at Shengjin Lake, China, using Illumina high-throughput sequencing technology (Mi-Seq platform).

Results

Our results revealed that Firmicutes, Actinobacteria, Proteobacteria, Bacteroidetes and Chloroflexi were the dominant bacterial phyla in both hosts. The gut bacterial community composition differed significantly between sympatric Hooded Cranes and Domestic Geese. However, the hosts exhibited little variation in gut bacterial alpha-diversity. The relative abundance of Firmicutes was significantly higher in the guts of the Hooded Cranes, while the relative abundances of Actinobacteria, Proteobacteria, Bacteroidete and Chloroflexi were significantly higher in guts of Domestic Geese. Moreover, a total of 132 potential pathogenic operational taxonomic units (OTUs) were detected in guts of Hooded Cranes and Domestic Geese, and 13 pathogenic OTUs (9.8%) were found in both host guts. Pathogenic bacterial community composition and diversity differed significantly between hosts.

Conclusions

The results showed that the gut bacterial community composition differs significantly between sympatric Hooded Cranes and Domestic Geese. In addition, potential pathogens were detected in the guts of both Hooded Cranes and Domestic Geese, with 13 pathogenic OTUs overlapping between the two hosts, suggesting that more attention should be paid to wild birds and poultry that might increase the risk of disease transmission in conspecifics and other mixed species.

Keywords: High-throughput sequencing, Hooded Crane, Pathogen, Poultry, Intestinal microbiota

References(76)

Alm EW, Daniels-Witt QR, Learman DR, Ryu H, Jordan DW, Gehring TM, et al. Potential for gulls to transport bacteria from human waste sites to beaches. Sci Total Environ. 2018;615:123-30.

Bortoluzzi C, Lumpkins B, Mathis GF, Franca M, King WD, Graugnard DE, et al. Zinc source modulates intestinal inflammation and intestinal integrity of broiler chickens challenged with coccidia and Clostridium perfringens. Poult Sci. 2019;98:2211-9.

Bottone EJ. Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev. 2010;23:382-98.

Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QⅡME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335-6.

Caron A, De Garine-Wichatitsky M, Gaidet N, Chiweshe N, Cumming GS. Estimating dynamic risk factors for pathogen transmission using community-level bird census data at the wildlife/domestic interface. Ecol Soc. 2010;15:299-305.

Chen SX, Wang Y, Chen FY, Yang HC, Gan MH, Zheng SJ. A highly pathogenic strain of Staphylococcus sciuri caused fatal exudative epidermitis in piglets. PLoS ONE. 2007;2:1-6.

Chen JY, Zhou LZ, Zhou B, Xu RX, Zhu WZ, Xu WB. Seasonal dynamics of wintering waterbirds in two shallow lakes along Yangtze River in Anhui Province. Zool Res. 2011;32:540-8.

Chevalier C, Stojanovic O, Colin DJ, Suarez-Zamorano N, Tarallo V, Veyrat-Durebex C, et al. Gut microbiota orchestrates energy homeostasis during cold. Cell. 2015;163:1360-74.

Craven SE, Stern NJ, Line E, Bailey JS, Cox NA, Fedorka-Cray P. Determination of the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in wild birds near broiler chicken houses by sampling intestinal droppings. Avian Dis. 2000;44:715-20.

Curtis SK, Kothary MH, Blodgett RJ, Raybourne RB, Ziobro GC, Tall BD. Rugosity in Grimontia hollisae. Appl Environ Microbiol. 2007;73:1215-24.

Delaunay E, Abat C, Rolain JM. Enterococcus cecorum human infection. France. New Microbes New Infect. 2015;7:50-1.

Deng P, Swanson KS. Gut microbiota of humans, dogs and cats: current knowledge and future opportunities and challenges. Br J Nutr. 2015;113:S6-17.

Desai SS, Harrison RA, Murphy MD. Capnocytophaga ochracea causing severe sepsis and purpura fulminans in an immunocompetent patient. J Infect. 2007;54:e107-109.

Dewar ML, Arnould JPY, Dann P, Trathan P, Groscolas R, Smith S. Interspecific variations in the gastrointestinal microbiota in penguins. MicrobiologyOpen. 2013;2:195-204.

Dufrêne M, Legendre P. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr. 1997;67:345-66.

Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-1.

Ekong PS, Fountain-Jones NM, Alkhamis MA. Spatiotemporal evolutionary epidemiology of H5N1 highly pathogenic avian influenza in West Africa and Nigeria, 2006-2015. Transbound Emerg Dis. 2018;65:e70-82.

Erbasan F. Brain abscess caused by Micrococcus luteus in a patient with systemic lupus erythematosus: case-based review. Rheumatol Int. 2018;38:2323-8.

Fan PX, Bian BL, Teng L, Nelson CD, Driver J, Elzo MA, et al. Host genetic effects upon the early gut microbiota in a bovine model with graduated spectrum of genetic variation. ISME J. 2020;14:302-17.

Fang J, Wang ZH, Zhao SQ, Li YK, Tang ZY, Yu D, et al. Biodiversity changes in the lakes of the Central Yangtze. Front Ecol Environ. 2006;4:369-77.

Ferraz V, McCarthy K, Smith D, Koornhof HJ. Rothia dentocariosa endocarditis and aortic root abscess. J Infect. 1998;37:292-5.

Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol. 2008;6:121-31.

Fox AD, Cao L, Zhang Y, Barter M, Zhao MJ, Meng FJ, et al. Declines in the tuber feeding waterbird guild at Shengjin Lake national nature reserve, China-a barometer of submerged macrophyte collapse. Aquat Conserv-Mar Freshw Ecosyst. 2011;21:82-91.

Galen SC, Witt CC. Diverse avian malaria and other haemosporidian parasites in Andean house wrens: evidence for regional co-diversification by host switching. J Avian Biol. 2014;45:374-86.

Grond K, Ryu H, Baker AJ, Domingo JWS, Buehler DM. Gastro-intestinal microbiota of two migratory shorebird species during spring migration staging in Delaware Bay, USA. J Ornithol. 2014;155:969-77.

Grond K, Lanctot RB, Jumpponen A, Sandercock BK. Recruitment and establishment of the gut microbiome in arctic shorebirds. FEMS Microbiol Ecol. 2017;93:142.

Grond K, Sandercock BK, Jumpponen A, Zeglin LH. The avian gut microbiota: community, physiology and function in wild birds. J Avian Biol. 2018;49:e01788.

He SD, Zhang ZY, Sun HJ, Zhu YC, Cao XD, Ye YK, et al. Potential effects of rapeseed peptide Maillard reaction products on aging-related disorder attenuation and gut microbiota modulation in d-galactose induced aging mice. Food Funct. 2019;10:4291-303.

Hird SM, Carstens BC, Cardiff S, Dittmann DL, Brumfield RT. Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood parasitic Brown-headed Cowbird (Molothrus ater). PeerJ. 2014;2:e321.

Hsueh PR, Teng LJ, Yang PC, Wang SK, Chang SC, Ho SW, et al. Bacteremia caused by Arcobacter cryaerophilus 1B. J Clin Microbiol. 1997;35:489-91.

Jiao SW, Guo YM, Huettmann F, Lei GC. Nest-site selection analysis of hooded crane (Grus monacha) in northeastern china based on a multivariate ensemble model. Zool Sci. 2014;31:430-7.

Jourdain E, Gauthier-Clerc M, Bicout DJ, Sabatier P. Bird migration routes and risk for pathogen dispersion into western mediterranean wetlands. Emerg Infect Dis. 2007;13:365-72.

Jung A, Chen LR, Suyemoto MM, Barnes HJ, Borst LB. A review of Enterococcus cecorum infection in poultry. Avian Dis. 2018;62:261-71.

Kira J, Isobe N. Helicobacter pylori infection and demyelinating disease of the central Nervous System. J Neuroimmunol. 2019;329:14-9.

Koziel N, Kukier E, Kwiatek K, Goldsztejn M. Clostridium perfringens-epidemiological importance and diagnostics. Med Weter. 2019;75:265-70.

LaFrentz BR, Garcia JC, Waldbieser GC, Evenhuis JP, Loch TP, Liles MR, et al. Identification of four distinct phylogenetic groups in Flavobacterium columnare with fish host associations. Front Microbiol. 2018;9:452-65.

Lalitha P, Srinivasan M, Prajna V. Rhodococcus ruber as a cause of keratitis. Cornea. 2006;25:238-9.

Lan PTN, Hayashi H, Sakamoto M, Benno Y. Phylogenetic analysis of cecal microbiota in chicken by the use of 16S rDNA clone libraries. Microbiol Immunol. 2002;46:371-82.

Lee SH, Kim KK, Rhyu IC, Koh S, Lee DS, Choi BK. Phenol/water extract of Treponema socranskii subsp. socranskii as an antagonist of Toll-like receptor 4 signalling. Microbiology. 2006;152:535-46.

Li G, Du XS, Zhou DF, Li CG, Huang LB, Zheng QK, et al. Emergence of pathogenic and multiple-antibiotic-resistant Macrococcus caseolyticus in commercial broiler chickens. Transbound Emerg Dis. 2018;65:1605-14.

Loy A, Pfann C, Steinberger M, Hanson B, Herp S, Brugiroux S, et al. Lifestyle and horizontal gene transfer-mediated evolution of Mucispirillum schaedleri, a core member of the murine gut microbiota. Msystems. 2017;2:e00171.

IUCN. The IUCN Red List of Threatened Species. 2020. Version 2019-3. https://www.iucnredlist.org.

Morgavi DP, Rathahao-Paris E, Popova M, Boccard J, Nielsen KF, Boudra H. Rumen microbial communities influence metabolic phenotypes in lambs. Front Microbiol. 2015;6:1060.

Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970-4.

Murakami Y, Hanazawa S, Tanaka S, Iwahashi H, Yamamoto Y, Fujisawa S. A possible mechanism of maxillofacial abscess formation: involvement of Porphyromonas endodontalis lipopolysaccharide via the expression of inflammatory cytokines. Oral Microbiol Immunol. 2001;16:321-5.

Nejrup RG, Licht TR, Hellgren LI. Fatty acid composition and phospholipid types used in infant formulas modifies the establishment of human gut bacteria in germ-free mice. Sci Rep. 2017;7:3975.

Nielsen HL. First report of Actinomyces europaeus bacteraemia result from a breast abscess in a 53-year-old man. New Microbes New Infect. 2015;7:21-2.

Nocera FP, Papulino C, Del Prete C, Palumbo V, Pasolini MP, De Martino L. Endometritis associated with Enterococcus casseliflavus in a mare: a case report. Asian Pac Trop Biomed. 2017;7:760-2.

Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan: community ecology package. Version 2.0-2. 2010.

Pantin-Jackwood MJ, Costa-Hurtado M, Shepherd E, DeJesus E, Smith D, Spackman E, et al. Pathogenicity and transmission of H5 and H7 highly pathogenic avian influenza viruses in mallards. J Virol. 2016;90:9967-82.

Pate M, Zolnir-Dovc M, Kusar D, Krt B, Spicic S, Cvetnic Z, et al. The first report of Mycobacterium celatum isolation from domestic pig (Sus scrofa domestica) and roe deer (Capreolus capreolus) and an overview of human infections in Slovenia. Vet Med Int. 2011;2011:432954.

Peng WJ, Dong B, Zhang SS, Huang H, Ye XK, Chen LN, et al. Research on rare cranes population response to land use change of nature wetland. J Indian Soc Remote Sens. 2018;46:1795-803.

Perofsky AC, Lewis RJ, Meyers LA. Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals. ISME J. 2019;13:50-63.

Ramey AM, Pearce JM, Flint PL, Ip HS, Derksen DV, Franson JC, et al. Intercontinental reassortment and genomic variation of low pathogenic avian influenza viruses isolated from northern pintails (Anas acuta) in Alaska: examining the evidence through space and time. Virology. 2010;401:179-89.

Reed C, Bruden D, Byrd KK, Veguilla V, Bruce M, Hurlburt D, et al. Characterizing wild bird contact and seropositivity to highly pathogenic avian influenza a (H5N1) virus in Alaskan residents. Influenza Other Resp. 2014;8:516-23.

Ruiu L. Brevibacillus laterosporus, a pathogen of invertebrates and a broad-spectrum antimicrobial species. Insects. 2013;4:476-92.

Sanders JG, Beichman AC, Roman J, Scott JJ, Emerson D, McCarthy JJ, et al. Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat Commun. 2015;6:8285.

Scheid PL, Lam TT, Sinsch U, Balczun C. Vermamoeba vermiformis as etiological agent of a painful ulcer close to the eye. Parasitol Res. 2019;118:1999-2004.

Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife. 2013;2:e01202.

Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:60.

Smith PA, Pizarro P, Ojeda P, Contreras J, Oyanedel S, Larenas J. Routes of entry of Piscirickettsia salmonis in rainbow trout Oncorhynchus mykiss. Dis Aquat Organ. 1999;37:165-72.

Stanley D, Denman SE, Hughes RJ, Geier MS, Crowley TM, Chen HL, et al. Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl Microbiol Biotechnol. 2012;96:1361-9.

Stanley D, Hughes RJ, Moore RJ. Microbiota of the chicken gastrointestinal tract: influence on health, productivity and disease. Appl Microbiol Biotechnol. 2014;98:4301-10.

Speirs LBM, Rice DTF, Petrovski S, Seviour RJ. The phylogeny, biodiversity, and ecology of the chloroflexi in activated sludge. Front Microbiol. 2019;10:2015.

Spence C, Wells WG, Smith CJ. Characterization of the primary starch utilization operon in the obligate anaerobe Bacteroides fragilis: regulation by carbon source and oxygen. J Bacteriol. 2006;188:4663-72.

Vendrell D, Balcazar JL, Ruiz-Zarzuela I, de Blas I, Girones O, Muzquiz JL. Lactococcus garvieae in fish: a review. Comp Immunol Microbiol Infect Dis. 2006;29:177-98.

Venugopal AA, Szpunar S, Johnson LB. Risk and prognostic factors among patients with bacteremia due to Eggerthella lenta. Anaerobe. 2012;18:475-8.

Waite DW, Eason DK, Taylor MW. Influence of hand rearing and bird age on the fecal microbiota of the critically endangered kakapo. Appl Environ Microbiol. 2014;80:4650-8.

Wilkinson TJ, Cowan AA, Vallin HE, Onime LA, Oyama LB, Cameron SJ, et al. Characterization of the microbiome along the gastrointestinal tract of growing turkeys. Front Microbiol. 2017;8:1-11.

Wise MG, Siragusa GR. Quantitative analysis of the intestinal bacterial community in one- to three-week-old commercially reared broiler chickens fed conventional or antibiotic-free vegetable-based diets. J Appl Microbiol. 2007;102:1138-49.

Xiang XJ, Zhang FL, Fu R, Yan SF, Zhou LZ. Significant differences in bacterial and potentially pathogenic communities between sympatric hooded crane and greater white-fronted goose. Front Microbiol. 2019;10:163.

Xiong JB, Wang K, Wu JF, Qiuqian LL, Yang KJ, Qian YX, et al. Changes in intestinal bacterial communities are closely associated with shrimp disease severity. Appl Microbiol Biotechnol. 2015;99:6911-9.

Yang L, Zhou LZ, Song YW. The effects of food abundance and disturbance on foraging flock patterns of the wintering hooded crane (Grus monacha). Avian Res. 2015;6:15.

Yang MJ, Song H, Sun LN, Yu ZL, Hu Z, Wang XL, et al. Effect of temperature on the microflora community composition in the digestive tract of the veined rapa whelk (Rapana venosa) revealed by 16S rRNA gene sequencing. Comp Biochem Phys D. 2019;29:145-53.

Zhao LL, Wang G, Siegel P, He C, Wang HZ, Zhao WJ, et al. Quantitative genetic background of the host influences gut microbiomes in chickens. Sci Rep. 2013;3:1163.

Zhu WF, Wei HJ, Chen L, Qiu RL, Fan ZY, Hu B, et al. Characterization of host plasminogen exploitation of Pasteurella multocida. Microb Pathog. 2019;129:74-7.

Publication history
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Publication history

Received: 21 December 2019
Accepted: 06 April 2020
Published: 30 April 2020
Issue date: January 2020

Copyright

© The Author(s) 2020.

Acknowledgements

Acknowledgements

We thank staff of Shenjin Lake National Nature Reserve for providing sample assistance in this study. We also thank Wei Chen, Weiqing Wang, Bingguo Dai, Jian Zhou, Xingran Wang, Zhengrong Zhu for helping us to collect samples.

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