Author:
Maidment Toby I.,Bryan Emily R.,Pyne Michael,Barnes Michele,Eccleston Sarah,Cunningham Samantha,Whitlock Emma,Redman Kelsie,Nicolson Vere,Beagley Kenneth W.,Pelzer Elise
Abstract
Abstract
Background
Captive koala breeding programmes are essential for long-term species management. However, breeding efficacy is frequently impacted by high neonatal mortality rates in otherwise healthy females. Loss of pouch young typically occurs during early lactation without prior complications during parturition and is often attributed to bacterial infection. While these infections are thought to originate from the maternal pouch, little is known about the microbial composition of koala pouches. As such, we characterised the koala pouch microbiome across the reproductive cycle and identified bacteria associated with mortality in a cohort of 39 captive animals housed at two facilities.
Results
Using 16S rRNA gene amplicon sequencing, we observed significant changes in pouch bacterial composition and diversity between reproductive time points, with the lowest diversity observed following parturition (Shannon entropy — 2.46). Of the 39 koalas initially sampled, 17 were successfully bred, after which seven animals lost pouch young (overall mortality rate — 41.18%). Compared to successful breeder pouches, which were largely dominated by Muribaculaceae (phylum — Bacteroidetes), unsuccessful breeder pouches exhibited persistent Enterobacteriaceae (phylum — Proteobacteria) dominance from early lactation until mortality occurred. We identified two species, Pluralibacter gergoviae and Klebsiella pneumoniae, which were associated with poor reproductive outcomes. In vitro antibiotic susceptibility testing identified resistance in both isolates to several antibiotics commonly used in koalas, with the former being multidrug resistant.
Conclusions
This study represents the first cultivation-independent characterisation of the koala pouch microbiota, and the first such investigation in marsupials associated with reproductive outcomes. Overall, our findings provide evidence that overgrowth of pathogenic organisms in the pouch during early development is associated with neonatal mortality in captive koalas. Our identification of previously unreported, multidrug resistant P. gergoviae strains linked to mortality also underscores the need for improved screening and monitoring procedures aimed at minimising neonatal mortality in future.
Publisher
Springer Science and Business Media LLC
Subject
Microbiology (medical),Microbiology
Reference71 articles.
1. Gonzalez-Astudillo V, Allavena R, McKinnon A, Larkin R, Henning J. Decline causes of koalas in South East Queensland, Australia: a 17-year retrospective study of mortality and morbidity”. Sci Reports. 2017;7:42587.
2. Adams-Hosking C, McBride MF, Baxter G, Burgman M, de Villiers D, Kavanagh R, et al. Use of expert knowledge to elicit population trends for the koala (Phascolarctos cinereus). Biodivers Res. 2016;22:249–62.
3. McAlpine C, Lunney D, Melzer A, Menkhorst P, Phillips S, Phalen D, et al. Conserving koalas: a review of the contrasting regional trends, outlooks and policy challenges. Biol Conserv. 2015;192:226–36.
4. Nyari S, Waugh CA, Dong J, Quigley BL, Hanger J, Loader J, et al. Epidemiology of chlamydial infection and disease in a free-ranging koala (Phascolarctos cinereus) population. PLoS ONE. 2017;12:e0190114.
5. McCallum H, Kerlin DH, Ellis W, Carrick F. Assessing the significance of endemic disease in conservation—koalas, chlamydia, and koala retrovirus as a case study. Conserv Letters. 2018;11:e12425.