Characterization of the juvenile koala gut microbiome across wild populations

Abstract

In this study we compared the faecal microbiomes of wild joey koalas (Phascolarctos cinereus) to those of adults, including their mothers, to establish whether gut microbiome maturation and inheritance in the wild is comparable to that seen in captivity. Our findings suggest that joey koala microbiomes slowly shift towards an adult assemblage between 6 and 12 months of age, as the microbiomes of 9-month-old joeys were more similar to those of adults than those of 7-month-olds, but still distinct. At the phylum level, differences between joeys and adults were broadly consistent with those in captivity, with Firmicutes increasing in relative abundance over the joeys' development and Proteobacteria decreasing. Of the fibre-degrading genes that increased in abundance over the development of captive joeys, those involved in hemicellulose and cellulose degradation, but not pectin degradation, were also generally found in higher abundance in adult wild koalas compared to 7-month-olds. Greater maternal inheritance of the faecal microbiome was seen in wild than in captive koalas, presumably due to the more solitary nature of wild koalas. This strong maternal inheritance of the gut microbiome could contribute to the development of localized differences in microbiome composition, population health and diet through spatial clustering of relatives.

Maternal inheritance of the koala gut microbiome and its compositional and functional maturation during juvenile development

“…This is because wild koalas are solitary, while captive koalas are co-housed at high density and pouch swapping is sometimes observed after initial pouch emergence. Indeed, in our companion paper (Blyton et al, 2022) we show a stronger maternal effect for wild joeys than observed in this study. Nonetheless, wild joeys did not always have microbiomes most similar to their mothers, suggesting that factors other than maternal transmission also play an important role in shaping the koala gut microbiome.…”

“…Despite this, three other species in this genus were at higher relative abundance in joey faeces after pap feeding. Similarly, the genus Tidjanibacter has been detected in human breast milk (Park and Yi, 2021) and members of this genera were enriched in joey faeces after pap feeding and in wild joeys in our companion paper (Blyton et al ., 2022). Furthermore, Bacteroides fragilis , which has also been isolated from human breast milk, utilizes milk oligosaccharides and is involved in the education of the innate immune system (Marcobal et al ., 2011; An et al ., 2014), was enriched in the joeys after pap feeding and in wild joeys.…”

“…One species from this family has been found at high relative abundance (~8%) in captive koalas (Shiffman et al ., 2017) and an inferred fibrolytic member of the same genus ( CAG‐873 ) also dominates the microbiomes of the koalas in this study. However, in studies of wild koalas, this family has only been found at low abundance (Blyton et al ., 2019; Brice et al ., 2019), including in the wild adult and joey koalas in our companion publication (Blyton et al ., 2022). Therefore, the relative importance of the family Muribaculaceae compared to families Lachnospiraceae and Ruminococcaceae in fibre degradation in koalas requires further investigation and may differ between captive and wild koalas.…”

Individuality and stability of the koala (Phascolarctos cinereus) faecal microbiota through time

“…Muribaculacaeae (Formerly S24-7) was found to be highly abundant in some Cleland koalas, but completely absent from Mountain Lagoon koalas. This taxon was previously identified at high relative abundance (>20%) from captive koalas located in Queensland and NSW ( Shiffman et al, 2017 ; Blyton et al, 2022b ), and yet was also not detected from wild koalas sampled from Cape Otway, Victoria ( Brice et al, 2019 ). Broader geographic sampling could determine whether this taxon is a marker for captivity, or endemic to specific koala populations.…”

“…This bacterium has received interest due to its positive association with koala survival during antibiotic treatment for Chlamydia ( Dahlhausen et al, 2018 ; Dahlhausen et al, 2020 ). However, these inter-population findings should be treated with caution, as our population-level comparison is confounded by captive (Cleland) vs wild (Mountain Lagoon), which can influence faecal microbiota composition in some vertebrate species ( Blyton et al, 2022b ; Kohl, Skopec & Dearing, 2014 ; Alberdi, Martin Bideguren & Aizpurua, 2021 ). These comparisons are also hindered by the small individual-level sample sizes ( n = 7 for Cleland, n = 5 for Mountain Lagoon).…”