Bacterial community composition in Adélie (Pygoscelis adeliae) and Chinstrap (Pygoscelis antarctica) Penguin stomach contents from Signy Island, South Orkney Islands
- 142 Downloads
Penguin stomach microbiota and its variability are important as these microbes may contribute to the fitness of the host birds and their chicks, and influence the microbial ecosystem of the surrounding soils. However, there is relatively little knowledge in this area, with the majority of studies focused on their deposited faeces. Here we investigated whether similar foraging strategies in adjacent colonies of different penguin species lead to similar temporarily conserved stomach microbiota. To do this, we studied the inter- and intra-specific variations in bacterial community composition in the stomach contents of sympatrically breeding Adélie (Pygoscelis adeliae) and Chinstrap (Pygoscelis antarctica) Penguins, which consumed a diet of 100% Antarctic krill (Euphausia superba) under a similar foraging regime on Signy Island (maritime Antarctic), using a high-throughput DNA sequencing approach. Our data show that Adélie and Chinstrap Penguins shared 23–63% similarity in the stomach bacterial community composition, with no significant differences observed in the α-diversity or the assemblages of frequently encountered groups of operational taxonomic units (OTUs). The most frequently encountered OTUs that were shared between the species represented members of the phyla Fusobacteria, Firmicutes, Tenericutes and Proteobacteria. OTUs which were unique to individual birds and to single species formed approximately half of the communities identified, suggesting that stomach microbiota variability can occur in penguins that forage and breed under similar environmental conditions.
KeywordsAntarctic High-throughput sequencing Internal gut Inter-individual Inter-specific Microbiota
This study was funded by the Sultan Mizan Antarctic Research Foundation (YPASM) and the National Antarctic Research Centre, University of Malaya Research Grant (UMRG: RP007-2012A). Laboratory resources were provided by British Antarctic Survey (BAS) and Northumbria University. We thank Stacey Adlard for her assistance in the field sampling. We also thank the editor and three anonymous reviewers for their constructive comments. Wen Chyin Yew is a recipient of MyBrain scholarship (MyPhD) funded by the Ministry of Higher Education Malaysia. Peter Convey and Michael J Dunn are supported by NERC core funding to the BAS “Biodiversity, Evolution and Adaptation” and “Ecosystems” teams, respectively. This paper also contributes to the Scientific Committee on Antarctic Research “State of the Antarctic Ecosystem” research programme (AntEco).
Compliance with ethical standards
All procedures involving animals followed internationally recognised CCAMLR CEMP standard methods and were in accordance with the ethical standards of the British Antarctic Survey.
Conflict of interest
The authors declare no competing interests.
- Banks JC, Cary SC, Hogg ID (2009) The phylogeography of Adélie Penguin faecal flora. Environ Microbiol 11:577–588Google Scholar
- 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. doi: 10.1371/journal.pone.0153215 CrossRefPubMedPubMedCentralGoogle Scholar
- Bjerrum L, Engberg RM, Leser TD, Jensen BB, Finster K, Pedersen K (2006) Microbial community composition of the ileum and cecum of broiler chickens as revealed by molecular and culture-based techniques. Poult Sci 85:1151–1164Google Scholar
- Boersma PD, Rebstock GA (2014) Climate change increases reproductive failure in Magellanic Penguins. PLoS ONE 9:e85602. doi: 10.1371/journal.pone.0085602
- Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
- CCAMLR (2003) CEMP standard methods. CCAMLR, HobartGoogle Scholar
- Gregersen RH, Neubauer C, Christensen H, Bojesen AM, Hess M, Bisgaard M (2009) Comparative studies on [Pasteurella] testudinis and [P.] testudinis-like bacteria and proposal of Chelonobacter oris gen. nov., sp. nov. as a new member of the family Pasteurellaceae. Int J Syst Evol Microbiol 59:1583–1588CrossRefPubMedGoogle Scholar
- Hughes JB, Bohannan BJM (2004) Section 7 update: application of ecological diversity statistics in microbial ecology. In: Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans AD, van Elsas JD (eds) Molecular microbial ecology manual, 2nd edn. Springer Netherlands, Dordrecht, pp 3223–3246Google Scholar
- Irgens RL, Gosink JJ, Staley JT (1996) Polaromonas vacuolata gen. nov., sp. nov., a psychrophilic, marine, gas vacuolate bacterium from Antarctica. Int J Syst Evol Microbiol 46:822–826Google Scholar
- Kyle PD, Kyle GZ (1993) An evaluation of the role of microbial flora in the salivary transfer technique for hand-rearing Chimney Swifts. Wildl Rehabil 8:65–71Google Scholar
- Lynnes A, Reid K, Croxall J, Trathan P (2002) Conflict or co-existence? Foraging distribution and competition for prey between Adélie and Chinstrap Penguins. Mar Biol 141:1165–1174Google Scholar
- Lynnes AS, Reid K, Croxall JP (2004) Diet and reproductive success of Adélie and Chinstrap Penguins: linking response of predators to prey population dynamics. Polar Biol 27:544–554Google Scholar
- Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server: a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi: 10.1186/1471-2105-9-386
- Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling tree swallows. The Auk 116:947–956Google Scholar
- Soucek Z, Mushin R (1970) Gastrointestinal bacteria of certain Antarctic birds and mammals. Appl Environ Microbiol 20:561–566Google Scholar
- Strong T, Dowd S, Gutierrez AF, Molnar D, Coffman J (2013) Amplicon pyrosequencing and ion torrent sequencing of wild duck eubacterial microbiome from fecal samples reveals numerous species linked to human and animal diseases [version 2; referees: 3 approved with reservations]. F1000Research 2:224. doi: 10.12688/f1000research.2-224.v2
- Thouzeau C, Maho YL, Froget G, Sabatier L, Le Bohec C, Hoffmann JA, Bulet P (2003b) Spheniscins, avian β-defensins in preserved stomach contents of the King Penguin, Aptenodytes patagonicus. J Biol Chem 278:51053–51058Google Scholar
- Ugolini FC (1972) Ornithogenic soils of Antarctica. In: Llano GA (ed) Antarctic terrestrial biology. American Geophysical Union, Washington. doi: 10.1002/9781118664667.ch9
- Van Der Wielen PWJJ, Biesterveld S, Notermans S, Hofstra H, Urlings BA, Van Knapen F (2000) Role of volatile fatty acids in development of the cecal microflora in broiler chickens during growth. Appl Environ Microbiol 66:2536–2540Google Scholar
- Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J.Field Ornithol 55:109-112. http://www.jstor.org/stable/4512864
- Yakimov MM, Giuliano L, Gentile G, Crisafi E, Chernikova TN, Abraham W-R, Lünsdorf H, Timmis KN, Golyshin PN (2003) Oleispira antarctica gen. nov., sp. nov., a novel hydrocarbonoclastic marine bacterium isolated from Antarctic coastal sea water. Int J Syst Evol Microbiol 53:779–785CrossRefPubMedGoogle Scholar