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

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 anatom...

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Veröffentlicht in:mBio 2021-08, Vol.12 (4), p.e0115321
Hauptverfasser: Zhu, Lifeng, Yang, Qinnan, Suhr Van Haute, Mallory J, Kok, Car Reen, Gomes-Neto, Joao Carlos, Pavlovikj, Natasha, Pillai, Resmi, Sinha, Rohita, Hassenstab, Haley, Mustoe, Aaryn, Moriyama, Etsuko N, Hutkins, Robert, French, Jeffrey, Benson, Andrew K
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container_issue 4
container_start_page e0115321
container_title mBio
container_volume 12
creator Zhu, Lifeng
Yang, Qinnan
Suhr Van Haute, Mallory J
Kok, Car Reen
Gomes-Neto, Joao Carlos
Pavlovikj, Natasha
Pillai, Resmi
Sinha, Rohita
Hassenstab, Haley
Mustoe, Aaryn
Moriyama, Etsuko N
Hutkins, Robert
French, Jeffrey
Benson, Andrew K
description 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 , , , , , and . Culturing and genomic analysis of the populations from adult animals identified four known marmoset-associated species ( , , , and ) and three unclassified taxa of that are phylogenetically distinct. Species-specific quantitative PCR (qPCR) confirmed that these same species of are abundant members of the microbiome throughout the lives of the animals. Genomic loci in each 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 that can support its unique ability to grow on arabinogalactan-rich tree gums, were species-specific. 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 species. Our studies show that several species of are dominant members of the captive marmoset microbiome throughout their life history. Metabolic capacities in genomes of the marmoset species suggest species-specific adaptations to different components of the captive marmoset diet, including the unique capacity in for degradation of gum arabic, suggesting that regular dietary exposure in captivity may be important for preserving gum-degrading species in the microbiome.
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Genomic loci in each 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 that can support its unique ability to grow on arabinogalactan-rich tree gums, were species-specific. 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 species. 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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 , , , , , and . Culturing and genomic analysis of the populations from adult animals identified four known marmoset-associated species ( , , , and ) and three unclassified taxa of that are phylogenetically distinct. Species-specific quantitative PCR (qPCR) confirmed that these same species of are abundant members of the microbiome throughout the lives of the animals. Genomic loci in each 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 that can support its unique ability to grow on arabinogalactan-rich tree gums, were species-specific. 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 species. Our studies show that several species of are dominant members of the captive marmoset microbiome throughout their life history. Metabolic capacities in genomes of the marmoset species suggest species-specific adaptations to different components of the captive marmoset diet, including the unique capacity in for degradation of gum arabic, suggesting that regular dietary exposure in captivity may be important for preserving gum-degrading species in the microbiome.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>34340536</pmid><doi>10.1128/mBio.01153-21</doi><tpages>24</tpages><orcidid>https://orcid.org/0000-0002-0589-4256</orcidid><orcidid>https://orcid.org/0000-0001-5304-1592</orcidid><oa>free_for_read</oa></addata></record>
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subjects Adaptation, Physiological - genetics
Animals
Bacteria - classification
Bacteria - genetics
Bifidobacterium - genetics
Bifidobacterium - physiology
Callithrix - microbiology
Diet
DNA, Bacterial - genetics
Feces - microbiology
Female
Gastrointestinal Microbiome - genetics
Gastrointestinal Microbiome - physiology
Genome, Bacterial
Gum Arabic - metabolism
Male
Microbial Ecology
Phylogeny
Research Article
Species Specificity
title 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
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