Journal Article

Captive Common Marmosets (Callithrix jacchus) Are Colonized throughout Their Lives by a Community of Bifidobacterium Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches

Sinha, Rohita, Kok, Car Reen, Pillai, Resmi, Yang, Qinnan, Pavlovikj, Natasha, Moriyama, Etsuko N., French, Jeffrey, Hassenstab, Haley, Zhu, Lifeng, Gomes-Neto, Joao Carlos, Mustoe, Aaryn, Benson, Andrew K., Suhr Van Haute, Mallory J., Hutkins, Robert

2021

Overview

Bifidobacterium species are recognized as important, beneficial microbes in the human gut microbiome, and their ability colonize individuals at different stages of life is influenced by poorly understood interactions between host, dietary, environmental, and ecological factors. The common marmoset is an emerging nonhuman primate model with a short maturation period, making this model amenable to study of the microbiome throughout a life history. The common marmoset ( Callithrix jacchus ) is an omnivorous New World primate whose diet in the wild includes large amounts of fruit, seeds, flowers, and a variety of lizards and invertebrates. Marmosets also feed heavily on tree gums and exudates, and they have evolved unique morphological and anatomical characteristics to facilitate gum feeding (gummivory). In this study, we characterized the fecal microbiomes of adult and infant animals from a captive population of common marmosets at the Callitrichid Research Center at the University of Nebraska at Omaha under their normal dietary and environmental conditions. The microbiomes of adult animals were dominated by species of Bifidobacterium , Bacteroides , Prevotella , Phascolarctobacterium , Megamonas , and Megasphaera . Culturing and genomic analysis of the Bifidobacterium populations from adult animals identified four known marmoset-associated species ( B. reuteri , B. aesculapii , B. myosotis , and B. hapali ) and three unclassified taxa of Bifidobacterium that are phylogenetically distinct. Species-specific quantitative PCR (qPCR) confirmed that these same species of Bifidobacterium are abundant members of the microbiome throughout the lives of the animals. Genomic loci in each Bifidobacterium species encode enzymes to support growth and major marmoset milk oligosaccharides during breastfeeding; however, metabolic islands that can support growth on complex polysaccharide substrates in the diets of captive adults (pectin, xyloglucan, and xylan), including loci in B. aesculapii that can support its unique ability to grow on arabinogalactan-rich tree gums, were species-specific. IMPORTANCE Bifidobacterium species are recognized as important, beneficial microbes in the human gut microbiome, and their ability colonize individuals at different stages of life is influenced by host, dietary, environmental, and ecological factors, which is poorly understood. The common marmoset is an emerging nonhuman primate model with a short maturation period, making this model amenable to study the microbiome throughout a life history. Features of the microbiome in captive marmosets are also shared with human gut microbiomes, including abundant populations of Bifidobacterium species. Our studies show that several species of Bifidobacterium are dominant members of the captive marmoset microbiome throughout their life history. Metabolic capacities in genomes of the marmoset Bifidobacterium species suggest species-specific adaptations to different components of the captive marmoset diet, including the unique capacity in B. aesculapii for degradation of gum arabic, suggesting that regular dietary exposure in captivity may be important for preserving gum-degrading species in the microbiome.

• Publisher: American Society for Microbiology
• Subject: Adaptation, Physiological - genetics / Animals / Arabinogalactan / Babies / Bacteria - classification / Bacteria - genetics / Bifidobacterium / Bifidobacterium - genetics / Bifidobacterium - physiology / Breast feeding / Callithrix - microbiology / Callithrix jacchus / Captivity / common marmoset / Diet / diet-driven gut microbiomes / DNA, Bacterial - genetics / Environmental conditions / Exudates / Feces - microbiology / Female / Fermentation / Gastrointestinal Microbiome - genetics / Gastrointestinal Microbiome - physiology / Genome, Bacterial / Genomic analysis / gum arabic / Gum Arabic - metabolism / gum-feeding specialists / Gums / Intestinal microflora / Life history / Male / Metabolism / Microbial Ecology / Microbiomes / Microbiota / Monkeys & apes / Oligosaccharides / Pectin / Phylogeny / Physical characteristics / Polysaccharides / Primates / Research Article / Species / Species Specificity / Taxonomy / Whole genome sequencing / Xylan / Xyloglucan