Gut microbes

Artwork copyright: Erin McKenney.

I have collected 143 fecal samples from 13 mammalian species housed at 4 different facilities, on a quest to investigate the microbial community dynamics associated with specific diets, gut morphology, evolutionary and life histories.

Host ecology and host history

A key question in microbiology is how complex communities assemble over time. I addressed this question by characterizing the effects of diet and phylogeny in highly diverged primate and carnivore species at the Duke Lemur Center and the Smithsonian National Zoo. By studying gut bacterial succession in captive lemurs, I was able to detect separate effects of host age, species, and diet on gut microbial membership. This was also the first study to incorporate nutritional, metagenomic, and metabolomic data across multiple species of primates. From birth, nursing lemurs exhibit variable communities dominated by opportunistic taxa that can digest milk oligosaccharides (i.e. Bifidobacteriales) and tolerate oxygen (i.e. many Proteobacteria). The introduction and regular consumption of solid foods, in particular plant carbohydrates, drive convergence toward the more stable, species-specific climax communities associated with healthy adulthood (McKenney et al. 2015).

Across lemurs in general, animals consuming more diverse (fibrous) diets tend to host more diverse gut microbes. It has long been predicted that diversity of food resources should predict diversity of species. This holds true in studies of animals, but I showed that it also holds true in guts. Yet the greater diversity hosted by leaf-eating lemurs is constrained, to specific microbes that are able to digest fiber and withstand anaerobic conditions (McKenney et al. 2017a). Thus, herbivory – which requires specific animal adaptations including increased gut complexity – also selects for specific microbial adaptations. Folivorous primates inhabit restricted habitat ranges in situ compared to their omnivorous counterparts, and also exhibit notoriously fragile health in captivity. My findings therefore have profound implications both for understanding the link between microbial variation and phenotypic flexibility, and also for informing husbandry.

To further explore the selective effects of fiber and phylogeny, I compared the bacterial communities associated with three bamboo specialists: the bamboo lemur (a primate), giant panda (a bear), and red panda (a relative of the raccoon). By comparing three herbivores with atypically short, simple gastrointestinal tracts, I was able to test whether differences in microbial diversity are results of long-term or short-term diets. Specifically – if ultimate factors like evolutionary history drive microbial diversity in the gut, then carnivores should be poorly adapted. I also discovered distinct classes of gut microbial membership, which differ in their relative abundance and are separately shaped by diet versus phylogeny. Generally, I found that differences in community structure are mediated by evolutionary differences. However, at the genus-level, bamboo lemurs share 6 times more membership with giant pandas and red pandas than with their sister species, further demonstrating the selective power of fiber across vast evolutionary distance (McKenney et al. 2017b).

Invasion

In addition to species-specific differences, every gut is susceptible to invasion. I quantified community disruption and characterized the process of secondary succession after healthy lemurs became infected with an intestinal pathogen (McKenney & Greene et al. 2017). This project builds on a long history of invasion research, but with specific ramifications for captive animals and human health. Infection with Cryptosporidium resulted in significantly decreased diversity and increased variation compared to healthy individuals. Bacterial membership was also altered, with enrichment of several taxa associated with disease in humans (i.e. Enterococcus and Desulfovibrio). Furthermore, my results demonstrate that the gut microbiome becomes more resilient with age, and that treatment with antimicrobials and fecal transfaunation consistently affect prognosis, with the latter facilitating a faster return to an individual’s pre-infection stable state. This finding in particular has informed husbandry and veterinary practices at the Duke Lemur Center – particularly in relation to the use of fecal transfaunation therapies to facilitate recovery­.