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RESEARCH ARTICLE (Open Access)

Pouch bacteria: an understudied and potentially important facet of marsupial reproduction

Toby Maidment A * and Raphael Eisenhofer B *
+ Author Affiliations
- Author Affiliations

A Queensland University of Technology, Centre for Immunology and Infection Control, Queensland Institute of Medical Research, 300 Herston Road, Brisbane, Qld 4001, Australia.

B Center for Evolutionary Hologenomics, Globe Institute, University of Copenhagen, DK-1353 Copenhagen, Denmark.




Toby Maidment is a research assistant at the Centre for Immunology and Infection Control, Queensland University of Technology. His current research focuses on koala reproductive diseases, host–microbiome interactions in the human FRT, and vaccine development. His major interests include Australian mammal conservation and microbial ecology.



Dr Raphael Eisenhofer is a postdoctoral researcher at the Globe Institute, University of Copenhagen, Denmark, and an adjunct assistant lecturer at the University of Adelaide. His research interest is studying the microbiomes of native Australian mammals, with the long-term goal of applying microorganisms to improve mammal conservation in Australia.

Microbiology Australia 44(1) 41-44 https://doi.org/10.1071/MA23010
Submitted: 16 January 2023  Accepted: 10 February 2023   Published: 3 March 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Australia is home to a rich biodiversity of marsupials that are found nowhere else. Unfortunately, many of these species are currently threatened with extinction due to introduced feral predators and other anthropogenic factors. There is growing recognition that host-associated microorganisms can play important roles for animal health, with billions of dollars currently being invested into human gut microbiome research and the development of microbiome-based therapeutics to improve human health. Can microorganisms also be harnessed to stem the tide of marsupial extinctions? In this review, we provide an overview of some of the challenges facing Australia’s marsupials, and our current understanding of the microbiology of the marsupial pouch. We also propose outstanding research questions pertaining to the marsupial pouch, which, if addressed, may provide actionable knowledge and novel microbial therapies that could help stem the tide of marsupial extinctions in Australia.


References

[1]  Woinarski, JCZ et al. (2015) Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc Natl Acad Sci USA 112, 4531–4540.
Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement.Crossref | GoogleScholarGoogle Scholar |

[2]  dos Reis, M et al. (2012) Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc R Soc B Biol Sci 279, 3491–3500.
Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny.Crossref | GoogleScholarGoogle Scholar |

[3]  Krause, WJ et al. (1978) Postnatal development of the epidermis in a marsupial, Didelphis virginiana. J Anat 125, 85–99.

[4]  Tyndale-Biscoe H, Renfree M (1987) Breeding biology of marsupials by family. In Reproductive Physiology of Marsupials. pp. 14–94. Cambridge University Press.

[5]  Australian Government. EPBC Act List of Threatened Fauna. https://www.environment.gov.au/cgi-bin/sprat/public/publicthreatenedlist.pl (accessed 14 January 2023)

[6]  Madden, D et al. (2018) Koala immunology and infectious diseases: how much can the koala bear? Dev Comp Immunol 82, 177–185.
Koala immunology and infectious diseases: how much can the koala bear?Crossref | GoogleScholarGoogle Scholar |

[7]  Peacock, D and Abbott, I (2014) When the ‘native cat’ would ‘plague’: historical hyperabundance in the quoll (Marsupialia : Dasyuridae) and an assessment of the role of disease, cats and foxes in its curtailment. Aust J Zool 62, 294–344.
When the ‘native cat’ would ‘plague’: historical hyperabundance in the quoll (Marsupialia : Dasyuridae) and an assessment of the role of disease, cats and foxes in its curtailment.Crossref | GoogleScholarGoogle Scholar |

[8]  Pye, RJ et al. (2016) Devil facial tumor disease. Vet Pathol 53, 726–736.
Devil facial tumor disease.Crossref | GoogleScholarGoogle Scholar |

[9]  Hughes, L (2011) Climate change and Australia: key vulnerable regions. Reg Environ Change 11, 189–195.
Climate change and Australia: key vulnerable regions.Crossref | GoogleScholarGoogle Scholar |

[10]  Johnston, S (2019) Challenges associated with the development and transfer of assisted breeding technology in marsupials and monotremes: lessons from the koala, wombat and short-beaked echidna. Reprod Fertil Dev 31, 1305–1314.
Challenges associated with the development and transfer of assisted breeding technology in marsupials and monotremes: lessons from the koala, wombat and short-beaked echidna.Crossref | GoogleScholarGoogle Scholar |

[11]  Seddon JM, Schultz B (2020) Koala conservation in Queensland, Australia: a role for assisted gene flow for genetic rescue? In Conservation Genetics in Mammals: Integrative Research Using Novel Approaches (Ortega J, Maldonado JE, eds). pp. 331–349. Springer International Publishing.

[12]  Hogan, LA et al. (2013) Wombat reproduction (Marsupialia; Vombatidae): an update and future directions for the development of artificial breeding technology. Reproduction 145, R157–R173.
Wombat reproduction (Marsupialia; Vombatidae): an update and future directions for the development of artificial breeding technology.Crossref | GoogleScholarGoogle Scholar |

[13]  O’Callaghan P (1996) Growth and mortality of koala pouch and back young. In Proceedings of the Australian Koala Foundation Annual Conference, Coolangatta, Qld, Australia. pp. 101–109. Australian Koala Foundation, Brisbane, Qld, Australia.

[14]  Hayward, MW et al. (2005) Mortality and survivorship of the quokka (Setonix brachyurus) (Macropodidae : Marsupialia) in the northern jarrah forest of Western Australia. Wildl Res 32, 715–722.
Mortality and survivorship of the quokka (Setonix brachyurus) (Macropodidae : Marsupialia) in the northern jarrah forest of Western Australia.Crossref | GoogleScholarGoogle Scholar |

[15]  Thompson, CK et al. (2015) Survival, age estimation and sexual maturity of pouch young of the brush-tailed bettong (Bettongia penicillata) in captivity. Aust Mammal 37, 29–38.
Survival, age estimation and sexual maturity of pouch young of the brush-tailed bettong (Bettongia penicillata) in captivity.Crossref | GoogleScholarGoogle Scholar |

[16]  McFall-Ngai, M et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110, 3229–3236.
Animals in a bacterial world, a new imperative for the life sciences.Crossref | GoogleScholarGoogle Scholar |

[17]  Trevelline, BK et al. (2019) Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc R Soc B Biol Sci 286, 20182448.
Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices.Crossref | GoogleScholarGoogle Scholar |

[18]  Comizzoli, P et al. (2021) Interactions between reproductive biology and microbiomes in wild animal species. Anim Microbiome 3, 87.
Interactions between reproductive biology and microbiomes in wild animal species.Crossref | GoogleScholarGoogle Scholar |

[19]  Yadav, M et al. (1972) The microbial flora of the gut of the pouch-young and the pouch of a marsupial, Setonix brachyurus. J Gen Microbiol 70, 437–442.
The microbial flora of the gut of the pouch-young and the pouch of a marsupial, Setonix brachyurus.Crossref | GoogleScholarGoogle Scholar |

[20]  Charlick, J et al. (1981) Quantitative alterations of the aerobic bacterial flora of the pouch of Setonix brachyurus (quokka) during oestrus, anoestrus, pregnancy and lactating anoestrus (pouch young). Aust J Exp Biol Med Sci 59, 743–751.
Quantitative alterations of the aerobic bacterial flora of the pouch of Setonix brachyurus (quokka) during oestrus, anoestrus, pregnancy and lactating anoestrus (pouch young).Crossref | GoogleScholarGoogle Scholar |

[21]  Osawa, R et al. (1992) Microflora of the pouch of the koala (Phascolarctos cinereus). J Wildl Dis 28, 276–280.
Microflora of the pouch of the koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar |

[22]  Old, JM and Deane, EM (1998) The effect of oestrus and the presence of pouch young on aerobic bacteria isolated from the pouch of the tammar wallaby, Macropus eugenii. Comp Immunol Microbiol Infect Dis 21, 237–245.
The effect of oestrus and the presence of pouch young on aerobic bacteria isolated from the pouch of the tammar wallaby, Macropus eugenii.Crossref | GoogleScholarGoogle Scholar |

[23]  Deakin, JE and Cooper, DW (2004) Characterisation of and immunity to the aerobic bacteria found in the pouch of the brushtail possum Trichosurus vulpecula. Comp Immunol Microbiol Infect Dis 27, 33–46.
Characterisation of and immunity to the aerobic bacteria found in the pouch of the brushtail possum Trichosurus vulpecula.Crossref | GoogleScholarGoogle Scholar |

[24]  Chhour, K-L et al. (2010) An observational study of the microbiome of the maternal pouch and saliva of the tammar wallaby, Macropus eugenii, and of the gastrointestinal tract of the pouch young. Microbiology 156, 798–808.
An observational study of the microbiome of the maternal pouch and saliva of the tammar wallaby, Macropus eugenii, and of the gastrointestinal tract of the pouch young.Crossref | GoogleScholarGoogle Scholar |

[25]  Cheng, Y et al. (2015) The Tasmanian devil microbiome—implications for conservation and management. Microbiome 3, 76.
The Tasmanian devil microbiome—implications for conservation and management.Crossref | GoogleScholarGoogle Scholar |

[26]  Peel, E et al. (2016) Cathelicidins in the Tasmanian devil (Sarcophilus harrisii). Sci Rep 6, 35019.
Cathelicidins in the Tasmanian devil (Sarcophilus harrisii).Crossref | GoogleScholarGoogle Scholar |

[27]  Eisenhofer, R et al. (2019) Contamination in low microbial biomass microbiome studies: issues and recommendations. Trends Microbiol 27, 105–117.
Contamination in low microbial biomass microbiome studies: issues and recommendations.Crossref | GoogleScholarGoogle Scholar |

[28]  Weiss, S et al. (2021) Host reproductive cycle influences the pouch microbiota of wild southern hairy-nosed wombats (Lasiorhinus latifrons). Anim Microbiome 3, 13.
Host reproductive cycle influences the pouch microbiota of wild southern hairy-nosed wombats (Lasiorhinus latifrons).Crossref | GoogleScholarGoogle Scholar |

[29]  Maidment T (2022) Characterisation of the pouch microbiome and association with reproductive outcomes in the koala (Phascolartos cinereus). MPh thesis, Queensland University of Technology.

[30]  Granato, ET et al. (2019) The evolution and ecology of bacterial warfare. Curr Biol 29, R521–R537.
The evolution and ecology of bacterial warfare.Crossref | GoogleScholarGoogle Scholar |

[31]  McKenzie, VJ et al. (2017) The effects of captivity on the mammalian gut microbiome. Integr Comp Biol 57, 690–704.
The effects of captivity on the mammalian gut microbiome.Crossref | GoogleScholarGoogle Scholar |