Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches

ABSTRACT 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 a...

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Autores principales:	Lifeng Zhu, Qinnan Yang, Mallory J. Suhr Van Haute, Car Reen Kok, Joao Carlos Gomes-Neto, Natasha Pavlovikj, Resmi Pillai, Rohita Sinha, Haley Hassenstab, Aaryn Mustoe, Etsuko N. Moriyama, Robert Hutkins, Jeffrey French, Andrew K. Benson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	common marmoset gum-feeding specialists Bifidobacterium diet-driven gut microbiomes gum arabic Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/80092b8f7e194e63a98d7f30d93c0e94
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spelling	oai:doaj.org-article:80092b8f7e194e63a98d7f30d93c0e942021-11-10T18:37:51ZCaptive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches10.1128/mBio.01153-212150-7511https://doaj.org/article/80092b8f7e194e63a98d7f30d93c0e942021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01153-21https://doaj.org/toc/2150-7511ABSTRACT 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.Lifeng ZhuQinnan YangMallory J. Suhr Van HauteCar Reen KokJoao Carlos Gomes-NetoNatasha PavlovikjResmi PillaiRohita SinhaHaley HassenstabAaryn MustoeEtsuko N. MoriyamaRobert HutkinsJeffrey FrenchAndrew K. BensonAmerican Society for Microbiologyarticlecommon marmosetgum-feeding specialistsBifidobacteriumdiet-driven gut microbiomesgum arabicMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	common marmoset gum-feeding specialists Bifidobacterium diet-driven gut microbiomes gum arabic Microbiology QR1-502
spellingShingle	common marmoset gum-feeding specialists Bifidobacterium diet-driven gut microbiomes gum arabic Microbiology QR1-502 Lifeng Zhu Qinnan Yang Mallory J. Suhr Van Haute Car Reen Kok Joao Carlos Gomes-Neto Natasha Pavlovikj Resmi Pillai Rohita Sinha Haley Hassenstab Aaryn Mustoe Etsuko N. Moriyama Robert Hutkins Jeffrey French Andrew K. Benson Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches
description	ABSTRACT 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.
format	article
author	Lifeng Zhu Qinnan Yang Mallory J. Suhr Van Haute Car Reen Kok Joao Carlos Gomes-Neto Natasha Pavlovikj Resmi Pillai Rohita Sinha Haley Hassenstab Aaryn Mustoe Etsuko N. Moriyama Robert Hutkins Jeffrey French Andrew K. Benson
author_facet	Lifeng Zhu Qinnan Yang Mallory J. Suhr Van Haute Car Reen Kok Joao Carlos Gomes-Neto Natasha Pavlovikj Resmi Pillai Rohita Sinha Haley Hassenstab Aaryn Mustoe Etsuko N. Moriyama Robert Hutkins Jeffrey French Andrew K. Benson
author_sort	Lifeng Zhu
title	Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches
title_short	Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches
title_full	Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches
title_fullStr	Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches
title_full_unstemmed	Captive Common Marmosets (<named-content content-type="genus-species">Callithrix jacchus</named-content>) Are Colonized throughout Their Lives by a Community of <italic toggle="yes">Bifidobacterium</italic> Species with Species-Specific Genomic Content That Can Support Adaptation to Distinct Metabolic Niches
title_sort	captive common marmosets (<named-content content-type="genus-species">callithrix jacchus</named-content>) are colonized throughout their lives by a community of <italic toggle="yes">bifidobacterium</italic> species with species-specific genomic content that can support adaptation to distinct metabolic niches
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/80092b8f7e194e63a98d7f30d93c0e94
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