Bacterial community composition in Adélie (Pygoscelis adeliae) and Chinstrap (Pygoscelis antarctica) Penguin stomach contents from Signy Island, South Orkney Islands

  • W. C. Yew
  • D. A. Pearce
  • M. J. Dunn
  • A. A. Samah
  • P. Convey
Original Paper

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.

Keywords

Antarctic High-throughput sequencing Internal gut Inter-individual Inter-specific Microbiota 

Supplementary material

300_2017_2162_MOESM1_ESM.xlsx (19 kb)
Supplementary material 1 (XLSX 19 kb)
300_2017_2162_MOESM2_ESM.xlsx (14 kb)
Supplementary material 2 (XLSX 13 kb)
300_2017_2162_MOESM3_ESM.xlsx (13 kb)
Supplementary material 3 (XLSX 13 kb)
300_2017_2162_MOESM4_ESM.xlsx (11 kb)
Supplementary material 4 (XLSX 12 kb)

References

  1. Banks JC, Cary SC, Hogg ID (2009) The phylogeography of Adélie Penguin faecal flora. Environ Microbiol 11:577–588Google Scholar
  2. 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
  3. Barnes EM, Impey CS, Cooper DM (1980) Manipulation of the crop and intestinal flora of the newly hatched chick. Am J Clin Nutr 33:2426–2433PubMedGoogle Scholar
  4. 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 103:732–737CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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
  6. Black CE (2016) A comprehensive review of the phenology of Pygoscelis penguins. Polar Biol 39:405–432CrossRefGoogle Scholar
  7. Boersma PD, Rebstock GA (2014) Climate change increases reproductive failure in Magellanic Penguins. PLoS ONE 9:e85602. doi:10.1371/journal.pone.0085602
  8. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997a) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078PubMedPubMedCentralGoogle Scholar
  10. 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 47:670–677CrossRefPubMedGoogle Scholar
  11. Brooke ML (2004) The food consumption of the world’s seabirds. Proc R Soc Lond B 271:246–248CrossRefGoogle Scholar
  12. 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
  13. 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 108:4516–4522CrossRefPubMedGoogle Scholar
  14. CCAMLR (2003) CEMP standard methods. CCAMLR, HobartGoogle Scholar
  15. 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 209:53–56CrossRefPubMedGoogle Scholar
  16. 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 151:287–297CrossRefGoogle Scholar
  17. Clarke A (1980) The biochemical composition of krill, Euphausia Superba Dana, from South Georgia. J Exp Mar Biol Ecol 43:221–236CrossRefGoogle Scholar
  18. Deagle BE, Jarman SN, Pemberton D, Gales NJ (2005) Genetic screening for prey in the gut contents from a giant squid. J Hered 96:417–423CrossRefPubMedGoogle Scholar
  19. 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 65:763–772CrossRefPubMedGoogle Scholar
  20. Dewar ML, Arnould JPY, Dann P, Trathan P, Groscolas R, Smith S (2013) Interspecific variations in the gastrointestinal microbiota in penguins. Microbiologyopen 2:195–204CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 CrossRefPubMedCentralGoogle Scholar
  23. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Forcada J, Trathan PN (2009) Penguin responses to climate change in the Southern Ocean. Glob Change Biol 15:1618–1630CrossRefGoogle Scholar
  25. 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 41:171–179CrossRefPubMedGoogle Scholar
  26. 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 59:147–157CrossRefPubMedGoogle Scholar
  27. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264CrossRefGoogle Scholar
  28. Goodrich JK, Di Rienzi SC, Poole AC, Koren O, Walters WA, Caporaso JG, Knight R, Ley RE (2014) Conducting a microbiome study. Cell 158:250–262CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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
  30. 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 155:969–977CrossRefGoogle Scholar
  31. 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 33:275–281CrossRefPubMedGoogle Scholar
  32. Heine JC, Speir TW (1989) Ornithogenic soils of the Cape Bird Adélie Penguin rookeries, Antarctica. Polar Biol 10:89–99CrossRefGoogle Scholar
  33. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hirsch PR, Mauchline TH, Clark IM (2010) Culture-independent molecular techniques for soil microbial ecology. Soil Biol Biochem 42:878–887CrossRefGoogle Scholar
  35. 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
  36. 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
  37. 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 21:306–314CrossRefPubMedGoogle Scholar
  38. Kelly MD, Lukaschewsky S, Anderson CG (1978) Bacterial flora of Antarctic krill (Euphasia superba) and some of their enzymatic properties. J Food Sci 43:1196–1197CrossRefGoogle Scholar
  39. Kohl KD (2012) Diversity and function of the avian gut microbiota. J Comp Physiol B 182:591–602CrossRefPubMedGoogle Scholar
  40. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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
  42. 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 69:6816–6824CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 36:510–516CrossRefGoogle Scholar
  44. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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
  46. 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
  47. 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 36:1347–1361CrossRefGoogle Scholar
  48. 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 50:19–28CrossRefPubMedGoogle Scholar
  49. 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 6:610–618CrossRefPubMedGoogle Scholar
  50. 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
  51. Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling tree swallows. The Auk 116:947–956Google Scholar
  52. Nicol S, Hosie GW (1993) Chitin production by krill. Biochem Syst Ecol 21:181–184CrossRefGoogle Scholar
  53. 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 8:686–696CrossRefPubMedGoogle Scholar
  54. Portrait V, Cottenceau G, Pons AM (2000) A Fusobacterium mortiferum strain produces a bacteriocin-like substance(s) inhibiting Salmonella enteritidis. Lett Appl Microbiol 31:115–117CrossRefPubMedGoogle Scholar
  55. 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 5:709–714CrossRefGoogle Scholar
  56. 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 59:4547–4554PubMedPubMedCentralGoogle Scholar
  57. 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 CrossRefGoogle Scholar
  58. Soucek Z, Mushin R (1970) Gastrointestinal bacteria of certain Antarctic birds and mammals. Appl Environ Microbiol 20:561–566Google Scholar
  59. 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 96:1361–1369CrossRefPubMedGoogle Scholar
  60. 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
  61. Suenaga H (2012) Targeted metagenomics: a high-resolution metagenomics approach for specific gene clusters in complex microbial communities. Environ Microbiol 14:13–22CrossRefPubMedGoogle Scholar
  62. Sun L, Xie Z, Zhao J (2000) Palaeoecology: A 3,000-year record of penguin populations. Nature 407:858. doi:10.1038/35038163 CrossRefPubMedGoogle Scholar
  63. 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 27:670–678CrossRefGoogle Scholar
  64. 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 250:279–289CrossRefGoogle Scholar
  65. 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 Google Scholar
  66. 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
  67. Ugolini FC (1972) Ornithogenic soils of Antarctica. In: Llano GA (ed) Antarctic terrestrial biology. American Geophysical Union, Washington. doi:10.1002/9781118664667.ch9
  68. 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
  69. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Waluda CM, Dunn MJ, Curtis ML, Fretwell PT (2014) Assessing penguin colony size and distribution using digital mapping and satellite remote sensing. Polar Biol 37:1849–1855CrossRefGoogle Scholar
  71. 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 17:296–304CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. 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 100:4201–4209CrossRefPubMedGoogle Scholar
  74. Wilson RP (1984) An improved stomach pump for penguins and other seabirds. J.Field Ornithol 55:109-112. http://www.jstor.org/stable/4512864
  75. 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
  76. 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 12:635–645CrossRefPubMedGoogle Scholar
  77. 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 13:245–254CrossRefGoogle Scholar
  78. 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 50:163–173CrossRefPubMedGoogle Scholar
  79. 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 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.National Antarctic Research Centre, Institute of Graduate StudiesUniversity of MalayaKuala LumpurMalaysia
  2. 2.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  3. 3.British Antarctic SurveyNERCCambridgeUK
  4. 4.Department of Applied Sciences, Faculty of Health and Life SciencesUniversity of Northumbria at NewcastleNewcastle upon TyneUK

Personalised recommendations