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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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. |
doi_str_mv | 10.1128/mBio.01153-21 |
format | Article |
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,
,
,
,
, 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.</description><identifier>ISSN: 2150-7511</identifier><identifier>EISSN: 2150-7511</identifier><identifier>DOI: 10.1128/mBio.01153-21</identifier><identifier>PMID: 34340536</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>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</subject><ispartof>mBio, 2021-08, Vol.12 (4), p.e0115321</ispartof><rights>Copyright © 2021 Zhu et al.</rights><rights>Copyright © 2021 Zhu et al. 2021 Zhu et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a383t-9cdc5c36aa74e56b87202d125e8cdbf713738e279ffd5cea8afc273df2cf9a3f3</citedby><cites>FETCH-LOGICAL-a383t-9cdc5c36aa74e56b87202d125e8cdbf713738e279ffd5cea8afc273df2cf9a3f3</cites><orcidid>0000-0002-0589-4256 ; 0000-0001-5304-1592</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/mBio.01153-21$$EPDF$$P50$$Gasm2$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/mBio.01153-21$$EHTML$$P50$$Gasm2$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,3188,27924,27925,52751,52752,52753,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34340536$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bello, Maria Gloria Dominguez</contributor><creatorcontrib>Zhu, Lifeng</creatorcontrib><creatorcontrib>Yang, Qinnan</creatorcontrib><creatorcontrib>Suhr Van Haute, Mallory J</creatorcontrib><creatorcontrib>Kok, Car Reen</creatorcontrib><creatorcontrib>Gomes-Neto, Joao Carlos</creatorcontrib><creatorcontrib>Pavlovikj, Natasha</creatorcontrib><creatorcontrib>Pillai, Resmi</creatorcontrib><creatorcontrib>Sinha, Rohita</creatorcontrib><creatorcontrib>Hassenstab, Haley</creatorcontrib><creatorcontrib>Mustoe, Aaryn</creatorcontrib><creatorcontrib>Moriyama, Etsuko N</creatorcontrib><creatorcontrib>Hutkins, Robert</creatorcontrib><creatorcontrib>French, Jeffrey</creatorcontrib><creatorcontrib>Benson, Andrew K</creatorcontrib><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</title><title>mBio</title><addtitle>mBio</addtitle><addtitle>mBio</addtitle><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.</description><subject>Adaptation, Physiological - genetics</subject><subject>Animals</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bifidobacterium - genetics</subject><subject>Bifidobacterium - physiology</subject><subject>Callithrix - microbiology</subject><subject>Diet</subject><subject>DNA, Bacterial - genetics</subject><subject>Feces - microbiology</subject><subject>Female</subject><subject>Gastrointestinal Microbiome - genetics</subject><subject>Gastrointestinal Microbiome - physiology</subject><subject>Genome, Bacterial</subject><subject>Gum Arabic - metabolism</subject><subject>Male</subject><subject>Microbial Ecology</subject><subject>Phylogeny</subject><subject>Research Article</subject><subject>Species Specificity</subject><issn>2150-7511</issn><issn>2150-7511</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kk9v1DAQxSMEolXpkSvyEZBSYnvzZy9I21AK0hYOLWdr4tjNrGI7sp3C9qvyZfDu0qoc8GU8mjc_Pes5y17T4oxS1nww5-jOCkpLnjP6LDtmtCzyuqT0-ZP7UXYawqZIh3Pa8OJldsQXfFGUvDrOfrcwRbxTpHXGOEuuwBsXVAzkbQvjiHHw-ItsQMphDu_Iyu-Uo7N4r3qShm6-Hdwcyc2g0JN1IgXSbQnsebPFuCVOk3PU2LsOZFQeZ0OuJyUxKX8m_kOT76tGSS6VdSbV1tmo7I4NkbRgyfU8Tc5HsuqTaYiY_EZHPmGIaGUkVypC58a0-Q3loMKr7IWGMajTv_Uk-_H54qb9kq-_X35tV-sceMNjvpS9LCWvAOqFKquuqVnBespK1ci-0zXlNW8Uq5da96VU0ICWrOa9ZlIvgWt-kn08cKe5M6qXybOHUUweDfitcIDi34nFQdy6O9EsioryKgHyA0B6F4JX-nGXFmIXtNgFLfZBC0aT_v1BD8EwsXGzt-l9_xW_eeruEf3wB_gfmaK4xg</recordid><startdate>20210831</startdate><enddate>20210831</enddate><creator>Zhu, Lifeng</creator><creator>Yang, Qinnan</creator><creator>Suhr Van Haute, Mallory J</creator><creator>Kok, Car Reen</creator><creator>Gomes-Neto, Joao Carlos</creator><creator>Pavlovikj, Natasha</creator><creator>Pillai, Resmi</creator><creator>Sinha, Rohita</creator><creator>Hassenstab, Haley</creator><creator>Mustoe, Aaryn</creator><creator>Moriyama, Etsuko N</creator><creator>Hutkins, Robert</creator><creator>French, Jeffrey</creator><creator>Benson, Andrew K</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0589-4256</orcidid><orcidid>https://orcid.org/0000-0001-5304-1592</orcidid></search><sort><creationdate>20210831</creationdate><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</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a383t-9cdc5c36aa74e56b87202d125e8cdbf713738e279ffd5cea8afc273df2cf9a3f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adaptation, Physiological - genetics</topic><topic>Animals</topic><topic>Bacteria - classification</topic><topic>Bacteria - genetics</topic><topic>Bifidobacterium - genetics</topic><topic>Bifidobacterium - physiology</topic><topic>Callithrix - microbiology</topic><topic>Diet</topic><topic>DNA, Bacterial - genetics</topic><topic>Feces - microbiology</topic><topic>Female</topic><topic>Gastrointestinal Microbiome - genetics</topic><topic>Gastrointestinal Microbiome - physiology</topic><topic>Genome, Bacterial</topic><topic>Gum Arabic - metabolism</topic><topic>Male</topic><topic>Microbial Ecology</topic><topic>Phylogeny</topic><topic>Research Article</topic><topic>Species Specificity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhu, Lifeng</creatorcontrib><creatorcontrib>Yang, Qinnan</creatorcontrib><creatorcontrib>Suhr Van Haute, Mallory J</creatorcontrib><creatorcontrib>Kok, Car Reen</creatorcontrib><creatorcontrib>Gomes-Neto, Joao Carlos</creatorcontrib><creatorcontrib>Pavlovikj, Natasha</creatorcontrib><creatorcontrib>Pillai, Resmi</creatorcontrib><creatorcontrib>Sinha, Rohita</creatorcontrib><creatorcontrib>Hassenstab, Haley</creatorcontrib><creatorcontrib>Mustoe, Aaryn</creatorcontrib><creatorcontrib>Moriyama, Etsuko N</creatorcontrib><creatorcontrib>Hutkins, Robert</creatorcontrib><creatorcontrib>French, Jeffrey</creatorcontrib><creatorcontrib>Benson, Andrew K</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>mBio</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhu, Lifeng</au><au>Yang, Qinnan</au><au>Suhr Van Haute, Mallory J</au><au>Kok, Car Reen</au><au>Gomes-Neto, Joao Carlos</au><au>Pavlovikj, Natasha</au><au>Pillai, Resmi</au><au>Sinha, Rohita</au><au>Hassenstab, Haley</au><au>Mustoe, Aaryn</au><au>Moriyama, Etsuko N</au><au>Hutkins, Robert</au><au>French, Jeffrey</au><au>Benson, Andrew K</au><au>Bello, Maria Gloria Dominguez</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>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</atitle><jtitle>mBio</jtitle><stitle>mBio</stitle><addtitle>mBio</addtitle><date>2021-08-31</date><risdate>2021</risdate><volume>12</volume><issue>4</issue><spage>e0115321</spage><pages>e0115321-</pages><issn>2150-7511</issn><eissn>2150-7511</eissn><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
,
,
,
,
, 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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