Microbial Genomics of a Host-Associated Commensal Bacterium in Fragmented Populations of Endangered Takahe
- 446 Downloads
Isolation of wildlife into fragmented populations as a consequence of anthropogenic-mediated environmental change may alter host-pathogen relationships. Our understanding of some of the epidemiological features of infectious disease in vulnerable populations can be enhanced by the use of commensal bacteria as a proxy for invasive pathogens in natural ecosystems. The distinctive population structure of a well-described meta-population of a New Zealand endangered flightless bird, the takahe (Porphyrio hochstetteri), provided a unique opportunity to investigate the influence of host isolation on enteric microbial diversity. The genomic epidemiology of a prevalent rail-associated endemic commensal bacterium was explored using core genome and ribosomal multilocus sequence typing (rMLST) of 70 Campylobacter sp. nova 1 isolated from one third of the takahe population resident in multiple locations. While there was evidence of recombination between lineages, bacterial divergence appears to have occurred and multivariate analysis of 52 rMLST genes revealed location-associated differentiation of C. sp. nova 1 sequence types. Our results indicate that fragmentation and anthropogenic manipulation of populations can influence host-microbial relationships, with potential implications for niche adaptation and the evolution of micro-organisms in remote environments. This study provides a novel framework in which to explore the complex genomic epidemiology of micro-organisms in wildlife populations.
KeywordsConservation Disease ecology Epidemiology Reserves Translocation
This study was funded by the Allan Wilson Centre. We would like to thank L. Howe, A. Reynolds, P. Marsh, J. Marshall, D. Wilkinson, G. Greaves, A. Wilson, B. Jackson, the friends of Tiritiri Matangi for assistance, Department of Conservation and the Maori community for their support.
Compliance with Ethical Standards
All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This article does not contain any studies with human participants performed by any of the authors.
Conflict of Interest
The authors declare that they have no conflict of interest.
- 8.Cowled BD, Ward MP, Laffan SW, Galea F, Garner MG, MacDonald AJ, Marsh I, Muellner P, Negus K, Quasim S, Woolnough AP, Sarre SD (2012) Integrating survey and molecular approaches to better understand wildlife disease ecology. PLoS One 7:e46310. doi: 10.1371/journal.pone.0046310 CrossRefPubMedPubMedCentralGoogle Scholar
- 16.Silvy NJ (2012) The wildlife techniques manual. Johns Hopkins University Press, Baltimore, USAGoogle Scholar
- 17.Wobeser GA (2006) Essentials of disease in wild animals. Blackwell, Ames, USAGoogle Scholar
- 20.Chiyo PI, Grieneisen LE, Wittemyer G, Moss CJ, Lee PC, Douglas-Hamilton I, Archie EA (2014) The influence of social structure, habitat, and host traits on the transmission of Escherichia coli in wild elephants. PLoS One 9:e93408. doi: 10.1371/journal.pone.0093408 CrossRefPubMedPubMedCentralGoogle Scholar
- 23.BirdLife International (2013) Porphyrio hochstetteri. www.iucnredlist.org. Accessed 24 February 2014
- 24.Wickes C, Crouchley D, Maxwell JM (2009) Takahe (Porphorio hochstetteri) recovery plan 2007–2012. Threatened species recovery plan 61. Department of Conservation, WellingtonGoogle Scholar
- 25.Ballance A (2001) Takahe: the bird that twice came back from the grave. In: The takahe: 50 years of conservation management and research. Otago University Press, Dunedin, New Zealand, pp 18–22Google Scholar
- 26.French NP, Yu S, Biggs P, Holland B, Fearnhead P, Binney B, Fox A, Grove-White D, Leigh JW, Miller W, Muellner P, Carter P (2014) Evolution of Campylobacter species in New Zealand. In: Sheppard SK (ed) Campylobacter ecology and evolution. Caister Academic Press, Norfolk, UK, pp 221–240Google Scholar
- 28.Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C, Colles FM, Wimalarathna H, Harrison OB, Sheppard SK, Cody AJ, Maiden MC (2012) Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158:1005–1015CrossRefPubMedPubMedCentralGoogle Scholar
- 29.Stevenson M (2014) epiR: an R package for the analysis of epidemiological data.Google Scholar
- 30.Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
- 38.Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E Ltd, Plymouth, UKGoogle Scholar
- 39.Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, UKGoogle Scholar
- 41.Manly BFJ (2007) Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall/ CRC, Boca Raton, FLGoogle Scholar
- 42.Biek R, O’Hare A, Wright D, Mallon T, McCormick C, Orton RJ, McDowell S, Trewby H, Skuce RA, Kao RR (2012) Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badger populations. PLoS Pathog 8:e1003008. doi: 10.1371/journal.ppat.1003008 CrossRefPubMedPubMedCentralGoogle Scholar
- 45.Trewick SA, Worthy TH (2001) Origins and prehistoric ecology of takahe based on morphometric, molecular, and fossil data. In: Lee WG, Jamieson IG (eds) The Takahe: 50 years of conservation management and research. Otago University Press, Dunedin, New Zealand, pp 31–48Google Scholar
- 48.Jaros P, Cookson AL, Campbell DM, Duncan GE, Prattley D, Carter P, Besser TE, Shringi S, Hathaway S, Marshall JC, French NP (2014) Geographic divergence of bovine and human shiga toxin-producing Escherichia coli O157:H7 genotypes, New Zealand. Emerg Infect Dis 20:1980–1989CrossRefPubMedPubMedCentralGoogle Scholar
- 51.Ryan CJ, Jamieson IG (1998) Estimating the home range and carrying capacity for takahe on predator free offshore islands: implications for future management. N Z J Ecol 22:17–24Google Scholar
- 57.Woodford MH (1993) International disease implications for wildlife translocation. J Zoo Wildl Med 24:265–270Google Scholar
- 58.Waldenstrom J, Axelsson-Olsson D, Olsen B, Hasselquist D, Griekspoor P, Jansson L, Teneberg S, Svensson L, Ellstrom P (2010) Campylobacter jejuni colonization in wild birds: results from an infection experiment. PLoS One 5:e9082. doi: 10.1371/journal.pone.0009082 CrossRefPubMedPubMedCentralGoogle Scholar