The Koala (Phascolarctos cinereus) faecal microbiome differs with diet in a wild population

Abstract

Background The diet of the koala (Phascolarctos cinereus) is comprised almost exclusively of foliage from the genus Eucalyptus (family Myrtaceae). Eucalyptus produces a wide variety of potentially toxic plant secondary metabolites which have evolved as chemical defences against herbivory. The koala is classified as an obligate dietary specialist, and although dietary specialisation is rare in mammalian herbivores, it has been found elsewhere to promote a highly-conserved but low-diversity gut microbiome. The gut microbes of dietary specialists have been found sometimes to enhance tolerance of dietary PSMs, facilitating competition-free access to food. Although the koala and its gut microbes have evolved together to utilise a low nutrient, potentially toxic diet, their gut microbiome has not previously been assessed in conjunction with diet quality. Thus, linking the two may provide new insights in to the ability of the koala to extract nutrients and detoxify their potentially toxic diet. Method The 16S rRNA gene was used to characterise the composition and diversity of faecal bacterial communities from a wild koala population (n = 32) comprising individuals that predominately eat either one of two different food species, one the strongly preferred and relatively nutritious species Eucalyptus viminalis, the other comprising the less preferred and less digestible species Eucalyptus obliqua. Results Alpha diversity indices indicated consistently and significantly lower diversity and richness in koalas eating E. viminalis. Assessment of beta diversity using both weighted and unweighted UniFrac matrices indicated that diet was a strong driver of both microbial community structure, and of microbial presence/absence across the combined koala population and when assessed independently. Further, principal coordinates analysis based on both the weighted and unweighted UniFrac matrices for the combined and separated populations, also revealed a separation linked to diet. During our analysis of the OTU tables we also detected a strong association between microbial community composition and host diet. We found that the phyla Bacteroidetes and Firmicutes were co-dominant in all faecal microbiomes, with Cyanobacteria also co-dominant in some individuals; however, the E. viminalis diet produced communities dominated by the genera Parabacteroides and/or Bacteroides, whereas the E. obliqua-associated diets were dominated by unidentified genera from the family Ruminococcaceae. Discussion We show that diet differences, even those caused by differential consumption of the foliage of two species from the same plant genus, can profoundly affect the gut microbiome of a specialist folivorous mammal, even amongst individuals in the same population. We identify key microbiota associated with each diet type and predict functions within the microbial community based on 80 previously identified Parabacteroides and Ruminococcaceae genomes.

When an iconic native animal is overabundant: The koala in southern Australia

“…Furthermore, koalas in these habitats exhibit high site fidelity and appear reluctant to move to alternate habitat types even when trees become completely defoliated (Whisson et al, ). Recent research into the koala's microbiome suggests that this may be due to koalas becoming highly specialized on a single food tree such that they may have limited ability to switch their diet to another food tree species (Blyton et al, ; Brice et al, ).…”

Isolation and sequence-based characterization of a koala symbiont: Lonepinella koalarum

“…Koalas ( Phascolarctos cinereus ) are arboreal marsupials that are highly specialized herbivores in that they feed almost exclusively on the foliage of select Eucalyptus species ( Moore & Foley, 2005 ; Callaghan et al, 2011 ). All Eucalyptus species contain chemical defenses against herbivory that include tannins, B-ring flavanones, phenolic compounds, terpenes, formylated phloroglucinols, cyanogenic glucosides and other plant secondary metabolites ( Lawler, Foley & Eschler, 2000 ; Gleadow et al, 2008 ; Brice et al, 2019 ; Liu et al, 2019 ). Plant chemical defenses can deter herbivores by affecting taste and/or digestibility of ingested material, with varying levels of toxic effects ( Brice et al, 2019 ).…”

“…All Eucalyptus species contain chemical defenses against herbivory that include tannins, B-ring flavanones, phenolic compounds, terpenes, formylated phloroglucinols, cyanogenic glucosides and other plant secondary metabolites ( Lawler, Foley & Eschler, 2000 ; Gleadow et al, 2008 ; Brice et al, 2019 ; Liu et al, 2019 ). Plant chemical defenses can deter herbivores by affecting taste and/or digestibility of ingested material, with varying levels of toxic effects ( Brice et al, 2019 ). These defenses and anti-nutrient compounds, which will be referred to generally as plant chemical defenses (for “PCDs”) hereafter, are very common, and there is well-established evidence that herbivores can overcome these defenses in their diet at least in part via PCD-degradation by their intestinal microbial communities ( Freeland & Janzen, 1974 ; Waterman et al, 1980 ; Hammer & Bowers, 2015 ; Kohl & Denise Dearing, 2016 ).…”

“…To date, the most compelling evidence for this is included in a recent study on the koala fecal microbiome, which identified several metabolic pathways and relevant bacterial species proposed to be important in detoxification processes ( Shiffman et al, 2017 ). The koala microbiome as a whole has shown to play an important role in macro nutrient digestion and fiber degradation ( Blyton et al, 2019 ; Brice et al, 2019 ). Moreover, there is evidence that the koala gastrointestinal microbiome can influence diet selection of individual hosts ( Blyton et al, 2019 ).…”

Polyphasic Characterisation of Cedecea colo sp. nov., a New Enteric Bacterium Isolated from the Koala Hindgut

“…In response to natural varying PSM concentrations, folivore species reduce their overall food intake, thereby regulating ingestion of harmful PSMs and avoiding intoxication [5][6][7]. Notwithstanding, animals subsisting entirely on eucalyptus foliage, such as koalas, rely on their native gut microbes for detoxification and the degradation of leaf components [8,9]. Microorganisms able to colonise such inhospitable environments may also withstand the extreme physicochemical conditions central to many industrial processes and thus are of significant interest to biotechnologists.…”