Variation in the Gut Microbiota of Common Marmosets: Differences with Colony of Origin and Integration

Abstract

Characterization of the gut microbiome may aid understanding and management of natural and experimental disease states in research animals, thereby promoting reproducibility. In this study, the rectal bacterial communities of three separate common marmoset (Callithrix jacchus) breeding colonies were defined using 16S rRNA sequencing of rectal swab samples. Study animals originated from two German colonies and a United States colony (JHU). The two German cohorts, previously fed the same diet, were imported into the JHU facility; they were then isolated, transitioned onto JHU diet, and then moved into rooms housing JHU animals. To dissect the contributions of diet and integration in shaping the rectal bacterial community, samples were collected from German origin marmosets upon JHU arrival (baseline), following diet transition (100 d), and following cohousing (390 d). Baseline and 390 d samples were collected from stably maintained JHU marmosets. Bacterial community composition was distinct between all three cohorts at baseline, suggesting that factors other than primary diet confer significant differences between captive populations. Beta-diversity of the animals from the two German colonies converged by 100 d but remained distinct from JHU sample beta-diversity throughout the 390-d study, indicating that diet had greater influence on bacterial community composition than did housing animals within the same room. Our results demonstrate substantial differences in gut bacteria between different captive marmoset colonies, with persistence of these differences following husbandry standardization and housing integration. Goals of rigor and reproducibility in research underscore the need to consider microbial differences between marmosets of diverse origin.ImportanceCharacterizing gut microbial populations is expected to promote health and enhance research reproducibility in animal studies. As use of common marmosets as animal models of human diseases expands, evaluating the marmoset gut bacterial community will be critical for interpreting research findings, especially as marmosets are prone to gastrointestinal inflammation. In this study, using 16S rRNA sequencing of rectal swab samples, we compared bacterial community among three captive colonies of marmosets at baseline and following importation of cohorts from two of the colonies into the third colony. Diet history had sustained influence on bacterial community composition, while housing the animals within the same room over a period of eight months did not appear to be a major factor. These persistent differences in marmoset gut bacterial community highlight the need for careful consideration of animal origin as a variable in marmoset research studies.

Best Practices for Microbiome Study Design in Companion Animal Research

“…Using a small number of individuals, or animals from a single research colony or location is not sufficient, as demonstrated by the large effects of research facility in mice (95) and primates (96), and the large variation across studies in companion animals (97). Ideally, sampling of many individuals of diverse genetic backgrounds from multiple locations is suggested (89).…”

“…Microbiome studies on other laboratory animals, including rodents and primates, suggests that results obtained from microbiome studies on colony animals might be difficult to replicate with animals from a different colony. Animals from different vendors or facilities, even if they are extremely similar genetically, have different microbiomes (95,96,147). The "vendor effect" can be larger than the effect of diet (95) and can impact multiple body systems (e.g., the immune system) (148,149).…”

Effects of enhanced insect feeding on the faecal microbiota and transcriptome of a family of captive common marmosets (Callithrix jacchus)

“…Studies revealed that the phyla Actinobacteria , Bacteroidetes , Firmicutes , Fusobacteria , and Proteobacteria are abundant in individuals without diseases [see 17 for a review], although high variability has been noted among facilities. The gut microbiome of primates is modulated by various factors, including diets [ 13 , 21 , 22 ], housing conditions [ 23 ], pairing [ 24 ], aging [ 15 ], and diseases [ 11 , 25 ]. Among them, diet is influential even for only a short period of time.…”