Abstract
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.
Similar content being viewed by others
References
Banks JC, Cary SC, Hogg ID (2009) The phylogeography of Adélie Penguin faecal flora. Environ Microbiol 11:577–588
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
Barnes EM, Impey CS, Cooper DM (1980) Manipulation of the crop and intestinal flora of the newly hatched chick. Am J Clin Nutr 33:2426–2433
Bik EM, Eckburg PB, Gill SR, Nelson KE, Purdom EA, Francois F, Perez-Perez G, Blaser MJ, Relman DA (2006) Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 103:732–737
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 85:1151–1164
Black CE (2016) A comprehensive review of the phenology of Pygoscelis penguins. Polar Biol 39:405–432
Boersma PD, Rebstock GA (2014) Climate change increases reproductive failure in Magellanic Penguins. PLoS ONE 9:e85602. doi:10.1371/journal.pone.0085602
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997a) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078
Bowman JP, McCammon SA, Brown JL, Nichols PD, McMeekin TA (1997b) Psychroserpens burtonensis gen. nov., sp. nov., and Gelidibacter algens gen. nov., sp. nov., psychrophilic bacteria isolated from Antarctic lacustrine and sea ice habitats. Int J Syst Bacteriol 47:670–677
Brooke ML (2004) The food consumption of the world’s seabirds. Proc R Soc Lond B 271:246–248
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 7:335–336
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108:4516–4522
CCAMLR (2003) CEMP standard methods. CCAMLR, Hobart
Chen HC, Chang CC, Mau WJ, Yen LS (2002) Evaluation of N-acetylchitooligosaccharides as the main carbon sources for the growth of intestinal bacteria. FEMS Microbiol Lett 209:53–56
Chen CY, Yu C, Chen SW, Chen BJ, Wang HT (2013) Effect of yeast with bacteriocin from rumen bacteria on growth performance, caecal flora, caecal fermentation and immunity function of broiler chicks. J Agric Sci 151:287–297
Clarke A (1980) The biochemical composition of krill, Euphausia Superba Dana, from South Georgia. J Exp Mar Biol Ecol 43:221–236
Deagle BE, Jarman SN, Pemberton D, Gales NJ (2005) Genetic screening for prey in the gut contents from a giant squid. J Hered 96:417–423
Delgado S, Cabrera-Rubio R, Mira A, Suárez A, Mayo B (2013) Microbiological survey of the human gastric ecosystem using culturing and pyrosequencing methods. Microb Ecol 65:763–772
Dewar ML, Arnould JPY, Dann P, Trathan P, Groscolas R, Smith S (2013) Interspecific variations in the gastrointestinal microbiota in penguins. Microbiologyopen 2:195–204
Dewar ML, Arnould JP, Krause L, Trathan P, Dann P, Smith SC (2014) Influence of fasting during moult on the faecal microbiota of penguins. PLoS ONE 9:e99996. doi:10.1371/journal.pone.0099996
Dickinson I, Goodall-Copestake W, Thorne MAS, Schlitt T, Ávila-Jiménez ML, Pearce DA (2016) Extremophiles in an Antarctic marine ecosystem. Microorganisms 4:8. doi:10.3390/microorganisms4010008
Dunn MJ, Jackson JA, Adlard S, Lynnes AS, Briggs DR, Fox D, Waluda CM (2016) Population size and decadal trends of three penguin species nesting at Signy Island, South Orkney Islands. PLoS ONE 11:e0164025. doi:10.1371/journal.pone.0164025
Forcada J, Trathan PN (2009) Penguin responses to climate change in the Southern Ocean. Glob Change Biol 15:1618–1630
Gong J, Forster RJ, Yu H, Chambers JR, Wheatcroft R, Sabour PM, Chen S (2002) Molecular analysis of bacterial populations in the ileum of broiler chickens and comparison with bacteria in the cecum. FEMS Microbiol Ecol 41:171–179
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
Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264
Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, Knight R, Ley RE (2014) Conducting a microbiome study. Cell 158:250–262
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 59:1583–1588
Grond K, Ryu H, Baker AJ, Santo Domingo JW, Buehler DM (2014) Gastro-intestinal microbiota of two migratory shorebird species during spring migration staging in Delaware Bay, USA. J Ornithol 155:969–977
Hammons S, Oh PL, Martínez I, Clark K, Schlegel VL, Sitorius E, Scheideler SE, Walter J (2010) A small variation in diet influences the Lactobacillus strain composition in the crop of broiler chickens. Syst Appl Microbiol 33:275–281
Heine JC, Speir TW (1989) Ornithogenic soils of the Cape Bird Adélie Penguin rookeries, Antarctica. Polar Biol 10:89–99
Hird SM, Carsten BC, Cardiff SW, Dittmann DL, Brumfield RT (2014) Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird (Molothrus ater). PeerJ 2:e321. doi:10.7717/peerj.321
Hirsch PR, Mauchline TH, Clark IM (2010) Culture-independent molecular techniques for soil microbial ecology. Soil Biol Biochem 42:878–887
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 3223–3246
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 46:822–826
Junge K, Gosink JJ, Hoppe HG, Staley JT (1998) Arthrobacter, Brachybacterium and Planococcus isolates identified from Antarctic sea ice brine. Description of Planococcus mcmeekinii, sp. nov. Syst Appl Microbiol 21:306–314
Kelly MD, Lukaschewsky S, Anderson CG (1978) Bacterial flora of Antarctic krill (Euphasia superba) and some of their enzymatic properties. J Food Sci 43:1196–1197
Kohl KD (2012) Diversity and function of the avian gut microbiota. J Comp Physiol B 182:591–602
Kreisinger J, Čížková D, Kropáčková L, Albrecht T (2015) Cloacal microbiome structure in a long-distance migratory bird assessed using deep 16sRNA pyrosequencing. PLoS ONE 10:e0137401. doi:10.1371/journal.pone.0137401
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 8:65–71
Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816–6824
Lucas FS, Heeb P (2005) Environmental factors shape cloacal bacterial assemblages in Great Tit Parus major and Blue Tit P. caeruleus nestlings. J Avian Biol 36:510–516
Luria CM, Amaral-Zettler LA, Ducklow HW, Rich JJ (2016) Seasonal succession of free-living bacterial communities in coastal waters of the western Antarctic Peninsula. Front Microbiol 7:1731. doi:10.3389/fmicb.2016.01731
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 141:1165–1174
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 27:544–554
Ma D, Zhu R, Ding W, Shen C, Chu H, Lin X (2013) Ex-situ enzyme activity and bacterial community diversity through soil depth profiles in penguin and seal colonies on Vestfold Hills, East Antarctica. Polar Biol 36:1347–1361
Maul JD, Gandhi JP, Farris JL (2005) Community-level physiological profiles of cloacal microbes in songbirds (Order: Passeriformes): variation due to host species, host diet, and habitat. Microb Ecol 50:19–28
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. The ISME Journal 6:610–618
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 116:947–956
Nicol S, Hosie GW (1993) Chitin production by krill. Biochem Syst Ecol 21:181–184
Passmore AJ, Jarman SN, Swadling KM, Kawaguchi S, McMinn A, Nicol S (2006) DNA as a dietary biomarker in Antarctic krill, Euphausia superba. Mar Biotechnol 8:686–696
Portrait V, Cottenceau G, Pons AM (2000) A Fusobacterium mortiferum strain produces a bacteriocin-like substance(s) inhibiting Salmonella enteritidis. Lett Appl Microbiol 31:115–117
Potti J, Moreno J, Yorio P, Briones V, García-Borboroglu P, Villar S, Ballesteros C (2002) Bacteria divert resources from growth for Magellanic Penguin chicks. Ecol Lett 5:709–714
Robrish SA, Oliver C, Thompson J (1991) Sugar metabolism by fusobacteria: regulation of transport, phosphorylation, and polymer formation by Fusobacterium mortiferum ATCC 25557. Infect Immun 59:4547–4554
Roggenbuck M, Schnell IB, Blom N, Bælum J, Bertelsen MF, Pontén TS (2014) The microbiome of New World vultures. Nat Commun 5:e5498. doi:10.1038/ncomms6498
Soucek Z, Mushin R (1970) Gastrointestinal bacteria of certain Antarctic birds and mammals. Appl Environ Microbiol 20:561–566
Stanley D, Denman SE, Hughes RJ, Geier MS, Crowley TM, Chen H, Haring VR, Moore RJ (2012) Intestinal microbiota associated with differential feed conversion efficiency in chickens. Appl Microbiol Biotechnol 96:1361–1369
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
Suenaga H (2012) Targeted metagenomics: a high-resolution metagenomics approach for specific gene clusters in complex microbial communities. Environ Microbiol 14:13–22
Sun L, Xie Z, Zhao J (2000) Palaeoecology: A 3,000-year record of penguin populations. Nature 407:858. doi:10.1038/35038163
Sun L, Zhu R, Yin X, Liu X, Xie Z, Wang Y (2004) A geochemical method for the reconstruction of the occupation history of a penguin colony in the maritime Antarctic. Polar Biol 27:670–678
Takahashi A, Dunn MJ, Trathan PN, Sato K, Naito Y, Croxall JP (2003) Foraging strategies of Chinstrap penguins at Signy Island, Antarctica: importance of benthic feeding on Antarctic krill. Mar Ecol Prog Ser 250:279–289
Thouzeau C, Froget G, Monteil H, Le Maho Y, Harf-Monteil C (2003a) Evidence of stress in bacteria associated with long-term preservation of food in the stomach of incubating King Penguins (Aptenodytes patagonicus). Polar Biol 26:115–123. doi:10.1007/s00300-002-0451-2
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 278:51053–51058
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 66:2536–2540
Waite DW, Taylor MW (2014) Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol 5:223. doi:10.3389/fmicb.2014.00223
Waluda CM, Dunn MJ, Curtis ML, Fretwell PT (2014) Assessing penguin colony size and distribution using digital mapping and satellite remote sensing. Polar Biol 37:1849–1855
Watanuki Y, Kato A, Naito Y, Robertson G, Robinson S (1997) Diving and foraging behaviour of Adélie Penguins in areas with and without fast sea-ice. Polar Biol 17:296–304
White MG, Conroy JWH (1975) Aspects of competition between pygoscelid penguins at Signy Island, South Orkney Islands. IBIS 117:371–373. doi:10.1111/j.1474-919X.1975.tb04224.x
Wilkinson N, Hughes RJ, Aspden WJ, Chapman J, Moore RJ, Stanley D (2016) The gastrointestinal tract microbiota of the Japanese quail, Coturnix japonica. Appl Microbiol Biotechnol 100:4201–4209
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 53:779–785
Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W, Schleifer K-H, Whitman WB, Euzéby J, Amann R, Rosselló-Móra R (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645
Zdanowski MK, Donachie SP (1993) Bacteria in the sea-ice zone between Elephant Island and the South Orkneys during the Polish sea-ice zone expedition, (December 1988 to January 1989). Polar Biol 13:245–254
Zdanowski MK, Weglenski P, Golik P, Sasin JM, Borsuk P, Zmuda MJ, Stankovic A (2004) Bacterial diversity in Adélie Penguin, Pygoscelis adeliae, guano: molecular and morpho-physiological approaches. FEMS Microbiol Ecol 50:163–173
Zhu R, Shi Y, Ma D, Wang C, Xu H, Chu H (2015) Bacterial diversity is strongly associated with historical penguin activity in an Antarctic lake sediment profile. Sci Rep 5:17231. doi:10.1038/srep17231
Acknowledgments
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
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.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yew, W.C., Pearce, D.A., Dunn, M.J. et al. Bacterial community composition in Adélie (Pygoscelis adeliae) and Chinstrap (Pygoscelis antarctica) Penguin stomach contents from Signy Island, South Orkney Islands. Polar Biol 40, 2517–2530 (2017). https://doi.org/10.1007/s00300-017-2162-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-017-2162-8