Links between bacteria derived from penguin guts and deposited guano and the surrounding soil microbiota
Penguins are an important indicator of marine ecosystem health and a major contributor of nutrients to terrestrial ecosystems in Antarctica. Their stomach microbiota is influenced by both the prey consumed and their foraging environment in the sea. As penguins feed at sea and breed on land, they might be expected to transfer microbes (e.g. prey-associated and marine bacteria) as well as nutrients from their stomachs while regurgitating food or in their guano to the surrounding terrestrial environment. However, most research attention to date has focused separately on the penguin gut microbiota (via cloacal/guano samples) and the terrestrial soil microbiota, and any relationship between them has yet to be established. Here, we analysed the bacterial communities in stomach regurgitates and cloacal swabs from the same individual birds, freshly deposited guano and rookery soils of two Pygoscelis penguins that breed sympatrically on Signy Island (South Orkney Islands, maritime Antarctic) using a high-throughput DNA sequencing method. Our data do not support the hypothesis that bacteria transferred from penguin guts and/or deposited guano make a significant contribution to the communities of the surrounding terrestrial microbial ecosystem. In both penguin species, composition of bacterial communities differed between the four sample types, with Jaccard similarities ranging between 10 and 36%. Assemblages of the dominant and co-occurring bacterial communities in rookery soils were either significantly negatively correlated or not correlated with the three other sample types. Sample-specific communities were also identified in this study, contributing around 63% of the identified diversity overall.
KeywordsAntarctic Bacterial input Microbial diversity Terrestrial environment
This study was funded by the Sultan Mizan Antarctic Research Foundation (YPASM) and University of Malaya Research Grant (UMRG: RP007-2012A). Laboratory resources were provided by British Antarctic Survey (BAS) and Northumbria University. We thank University of Malaya for supporting Visiting Professors David A. Pearce (under Visiting Professor Scheme) and Peter Convey (under Academic Icon Programme) to the National Antarctic Research Centre. 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
Conflict of interest
The authors declare that they have no conflict of interest.
All procedures involving animals followed internationally recognised CCAMLR CEMP standard methods and were in accordance with the ethical standards of the British Antarctic Survey.
- 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
- CCAMLR (2003) CEMP standard methods. CCAMLR, HobartGoogle Scholar
- Fowler J, Cohen L, Jarvis P (1998) Practical statistics for field biology. John Wiley and Sons, ChichesterGoogle 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 MG-RAST server: a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386. doi: 10.1186/1471-2105-9-386 CrossRefGoogle Scholar
- Trawińska B, Chmielowiec-Korzeniowska A, Nowakowicz-Dębek B, Tymczyna L, Bombik T, Pyrz M, Tymczyna-Sobotka M (2016) Evaluation of microbial contamination of feces and soil on a laying-hen farm depending on sampling site and season. Revista Brasileira de Zootecnia 45:190–194. doi: 10.1590/S1806-92902016000400007 CrossRefGoogle Scholar
- Wang NF, Zhang T, Zhang F, Wang ET, He JF, Ding H, Zhang BT, Liu J, Ran XB, Zang JY (2015) Diversity and structure of soil bacterial communities in the Fildes Region (maritime Antarctica) as revealed by 454 pyrosequencing. Front Microbiol 6:1188. doi: 10.3389/fmicb.2015.01188 PubMedPubMedCentralGoogle 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
- Yau S, Lauro FM, Williams TJ, DeMaere MZ, Brown MV, Rich J, Gibson JAE, Cavicchioli R (2013) Metagenomic insights into strategies of carbon conservation and unusual sulphur biogeochemistry in a hypersaline Antarctic lake. ISME J 7:1944–1961. doi: 10.1038/ismej.2013.69 CrossRefPubMedPubMedCentralGoogle Scholar