Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores
The rumen houses a diverse community that plays a major role in the digestion process in ruminants. Anaerobic gut fungi (AGF) are key contributors to plant digestion in the rumen. Here, we present a global amplicon-based survey of the rumen AGF mycobiome by examining 206 samples from 15 animal speci...
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| Veröffentlicht in: | Applied and environmental microbiology 2024-02, Vol.90 (2), p.e0149223 |
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| creator | Meili, Casey H TagElDein, Moustafa A Jones, Adrienne L Moon, Christina D Andrews, Catherine Kirk, Michelle R Janssen, Peter H J Yeoman, Carl Grace, Savannah Borgogna, Joanna-Lynn C Foote, Andrew P Nagy, Yosra I Kashef, Mona T Yassin, Aymen S Elshahed, Mostafa S Youssef, Noha H |
| description | The rumen houses a diverse community that plays a major role in the digestion process in ruminants. Anaerobic gut fungi (AGF) are key contributors to plant digestion in the rumen. Here, we present a global amplicon-based survey of the rumen AGF mycobiome by examining 206 samples from 15 animal species, 15 countries, and 6 continents. The rumen AGF mycobiome was highly diverse, with 81 out of 88 currently recognized AGF genera or candidate genera identified. However, only six genera (
NY9, and
) were present at >4% relative abundance. AGF diversity was higher in members of the families
and
compared to
. Community structure analysis identified a pattern of phylosymbiosis, where host family (10% of total variance) and species (13.5%) partially explained the rumen mycobiome composition. As well, diet composition (9%-19%), domestication (11.14%), and biogeography (14.1%) also partially explained AGF community structure; although sampling limitation, geographic range restrictions, and direct association between different factors hindered accurate elucidation of the relative contribution of each factor. Pairwise comparison of rumen and fecal samples obtained from the same subject (
= 13) demonstrated greater diversity and inter-sample variability in rumen versus fecal samples. The genera
and
were present in higher abundance in rumen samples, while
and
were enriched in fecal samples. Comparative analysis of global rumen and feces data sets revealed a similar pattern. Our results provide a global view of AGF community in the rumen and identify patterns of AGF variability between rumen and feces in herbivores Gastrointestinal (GI) tract.IMPORTANCERuminants are highly successful and economically important mammalian suborder. Ruminants are herbivores that digest plant material with the aid of microorganisms residing in their GI tract. In ruminants, the rumen compartment represents the most important location where microbially mediated plant digestion occurs, and is known to house a bewildering array of microbial diversity. An important component of the rumen microbiome is the anaerobic gut fungi (AGF), members of the phylum
. So far, studies examining AGF diversity have mostly employed fecal samples, and little is currently known regarding the identity of AGF residing in the rumen compartment, factors that impact the observed patterns of diversity and community structure of AGF in the rumen, and how AGF communities in the rumen compare to AGF communities in feces. Her |
| doi_str_mv | 10.1128/aem.01492-23 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10880628</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2921118056</sourcerecordid><originalsourceid>FETCH-LOGICAL-a404t-d85957d15fd30052ced13c99cb4a4213a3e20dbf38148ed3c9a0300540e007dd3</originalsourceid><addsrcrecordid>eNp1kUtrFTEYhoMo9ljduZYBNxWc-uUy5yQrKfVWKLjRdcgk35yTMjOpuRzpvzfTU-sFugof78NDXl5CXlI4pZTJdwanU6BCsZbxR2RFQcm243z9mKwAlGoZE3BEnqV0BQAC1vIpOeKSKSUpXxH_we8xJp9vGjO7xoZpKvNypRyLzSViE4YaGYyh97bZltwMZd76xs9N3mETy4Tzwvz0o7t1uDBhyt6ajK7ZYez9PkRMz8mTwYwJX9y9x-T7p4_fzr-0l18_X5yfXbZGgMitk53qNo52g-MAHbPoKLdK2V4YwSg3HBm4fuCSComuRgYWUAACbJzjx-T9wXtd-gmdxTlHM-rr6CcTb3QwXv-bzH6nt2GvKUgJayar4eTOEMOPUrvoySeL42hmDCVpphilVEK3rujr_9CrUOJc-1WKb6QUG7lQbw-UjSGliMP9byjoZURdR9S3I2rGK_7mgJs0sT_CB9hXf7e9F_9emP8CHmSmYg</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2937884786</pqid></control><display><type>article</type><title>Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores</title><source>MEDLINE</source><source>American Society for Microbiology Journals</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><creator>Meili, Casey H ; TagElDein, Moustafa A ; Jones, Adrienne L ; Moon, Christina D ; Andrews, Catherine ; Kirk, Michelle R ; Janssen, Peter H ; J Yeoman, Carl ; Grace, Savannah ; Borgogna, Joanna-Lynn C ; Foote, Andrew P ; Nagy, Yosra I ; Kashef, Mona T ; Yassin, Aymen S ; Elshahed, Mostafa S ; Youssef, Noha H</creator><contributor>Reguera, Gemma</contributor><creatorcontrib>Meili, Casey H ; TagElDein, Moustafa A ; Jones, Adrienne L ; Moon, Christina D ; Andrews, Catherine ; Kirk, Michelle R ; Janssen, Peter H ; J Yeoman, Carl ; Grace, Savannah ; Borgogna, Joanna-Lynn C ; Foote, Andrew P ; Nagy, Yosra I ; Kashef, Mona T ; Yassin, Aymen S ; Elshahed, Mostafa S ; Youssef, Noha H ; Reguera, Gemma</creatorcontrib><description>The rumen houses a diverse community that plays a major role in the digestion process in ruminants. Anaerobic gut fungi (AGF) are key contributors to plant digestion in the rumen. Here, we present a global amplicon-based survey of the rumen AGF mycobiome by examining 206 samples from 15 animal species, 15 countries, and 6 continents. The rumen AGF mycobiome was highly diverse, with 81 out of 88 currently recognized AGF genera or candidate genera identified. However, only six genera (
NY9, and
) were present at >4% relative abundance. AGF diversity was higher in members of the families
and
compared to
. Community structure analysis identified a pattern of phylosymbiosis, where host family (10% of total variance) and species (13.5%) partially explained the rumen mycobiome composition. As well, diet composition (9%-19%), domestication (11.14%), and biogeography (14.1%) also partially explained AGF community structure; although sampling limitation, geographic range restrictions, and direct association between different factors hindered accurate elucidation of the relative contribution of each factor. Pairwise comparison of rumen and fecal samples obtained from the same subject (
= 13) demonstrated greater diversity and inter-sample variability in rumen versus fecal samples. The genera
and
were present in higher abundance in rumen samples, while
and
were enriched in fecal samples. Comparative analysis of global rumen and feces data sets revealed a similar pattern. Our results provide a global view of AGF community in the rumen and identify patterns of AGF variability between rumen and feces in herbivores Gastrointestinal (GI) tract.IMPORTANCERuminants are highly successful and economically important mammalian suborder. Ruminants are herbivores that digest plant material with the aid of microorganisms residing in their GI tract. In ruminants, the rumen compartment represents the most important location where microbially mediated plant digestion occurs, and is known to house a bewildering array of microbial diversity. An important component of the rumen microbiome is the anaerobic gut fungi (AGF), members of the phylum
. So far, studies examining AGF diversity have mostly employed fecal samples, and little is currently known regarding the identity of AGF residing in the rumen compartment, factors that impact the observed patterns of diversity and community structure of AGF in the rumen, and how AGF communities in the rumen compare to AGF communities in feces. Here, we examined the rumen AGF diversity using an amplicon-based survey targeting a wide range of wild and domesticated ruminants (
= 206, 15 different animal species) obtained from 15 different countries. Our results demonstrate that while highly diverse, no new AGF genera were identified in the rumen mycobiome samples examined. Our analysis also indicate that animal host phylogeny, diet, biogeography, and domestication status could play a role in shaping AGF community structure. Finally, we demonstrate that a greater level of diversity and higher inter-sample variability was observed in rumen compared to fecal samples, with two genera (
and
) present in higher abundance in rumen samples, and two others (
and
) enriched in fecal samples. Our results provide a global view of the identity, diversity, and community structure of AGF in ruminants, elucidate factors impacting diversity and community structure of the rumen mycobiome, and identify patterns of AGF community variability between the rumen and feces in the herbivorous GI tract.</description><identifier>ISSN: 0099-2240</identifier><identifier>ISSN: 1098-5336</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/aem.01492-23</identifier><identifier>PMID: 38299813</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Abundance ; Anaerobic processes ; Anaerobiosis ; Animal species ; Animals ; Biogeography ; Caecomyces ; Community structure ; Comparative analysis ; Composition ; Cyllamyces ; Deer ; Digestion ; Digestive system ; Domestication ; Ecology ; Feces ; Fungi ; Fungi - genetics ; Gastrointestinal tract ; Herbivores ; Herbivory ; Humans ; Intestinal microflora ; Microbial Ecology ; Neocallimastix ; Orpinomyces ; Pattern analysis ; Piromyces ; Relative abundance ; Rumen ; Rumen - microbiology ; Ruminants ; Spotlight Selection ; Structural analysis ; Variability</subject><ispartof>Applied and environmental microbiology, 2024-02, Vol.90 (2), p.e0149223</ispartof><rights>Copyright © 2024 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Feb 2024</rights><rights>Copyright © 2024 American Society for Microbiology. 2024 American Society for Microbiology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a404t-d85957d15fd30052ced13c99cb4a4213a3e20dbf38148ed3c9a0300540e007dd3</cites><orcidid>0000-0002-1022-3502 ; 0000-0003-0379-3440 ; 0000-0002-4488-4042 ; 0000-0001-9159-3785 ; 0000-0001-9692-9559</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/aem.01492-23$$EPDF$$P50$$Gasm2$$H</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/aem.01492-23$$EHTML$$P50$$Gasm2$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,3188,27924,27925,52751,52752,52753,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38299813$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Reguera, Gemma</contributor><creatorcontrib>Meili, Casey H</creatorcontrib><creatorcontrib>TagElDein, Moustafa A</creatorcontrib><creatorcontrib>Jones, Adrienne L</creatorcontrib><creatorcontrib>Moon, Christina D</creatorcontrib><creatorcontrib>Andrews, Catherine</creatorcontrib><creatorcontrib>Kirk, Michelle R</creatorcontrib><creatorcontrib>Janssen, Peter H</creatorcontrib><creatorcontrib>J Yeoman, Carl</creatorcontrib><creatorcontrib>Grace, Savannah</creatorcontrib><creatorcontrib>Borgogna, Joanna-Lynn C</creatorcontrib><creatorcontrib>Foote, Andrew P</creatorcontrib><creatorcontrib>Nagy, Yosra I</creatorcontrib><creatorcontrib>Kashef, Mona T</creatorcontrib><creatorcontrib>Yassin, Aymen S</creatorcontrib><creatorcontrib>Elshahed, Mostafa S</creatorcontrib><creatorcontrib>Youssef, Noha H</creatorcontrib><title>Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>The rumen houses a diverse community that plays a major role in the digestion process in ruminants. Anaerobic gut fungi (AGF) are key contributors to plant digestion in the rumen. Here, we present a global amplicon-based survey of the rumen AGF mycobiome by examining 206 samples from 15 animal species, 15 countries, and 6 continents. The rumen AGF mycobiome was highly diverse, with 81 out of 88 currently recognized AGF genera or candidate genera identified. However, only six genera (
NY9, and
) were present at >4% relative abundance. AGF diversity was higher in members of the families
and
compared to
. Community structure analysis identified a pattern of phylosymbiosis, where host family (10% of total variance) and species (13.5%) partially explained the rumen mycobiome composition. As well, diet composition (9%-19%), domestication (11.14%), and biogeography (14.1%) also partially explained AGF community structure; although sampling limitation, geographic range restrictions, and direct association between different factors hindered accurate elucidation of the relative contribution of each factor. Pairwise comparison of rumen and fecal samples obtained from the same subject (
= 13) demonstrated greater diversity and inter-sample variability in rumen versus fecal samples. The genera
and
were present in higher abundance in rumen samples, while
and
were enriched in fecal samples. Comparative analysis of global rumen and feces data sets revealed a similar pattern. Our results provide a global view of AGF community in the rumen and identify patterns of AGF variability between rumen and feces in herbivores Gastrointestinal (GI) tract.IMPORTANCERuminants are highly successful and economically important mammalian suborder. Ruminants are herbivores that digest plant material with the aid of microorganisms residing in their GI tract. In ruminants, the rumen compartment represents the most important location where microbially mediated plant digestion occurs, and is known to house a bewildering array of microbial diversity. An important component of the rumen microbiome is the anaerobic gut fungi (AGF), members of the phylum
. So far, studies examining AGF diversity have mostly employed fecal samples, and little is currently known regarding the identity of AGF residing in the rumen compartment, factors that impact the observed patterns of diversity and community structure of AGF in the rumen, and how AGF communities in the rumen compare to AGF communities in feces. Here, we examined the rumen AGF diversity using an amplicon-based survey targeting a wide range of wild and domesticated ruminants (
= 206, 15 different animal species) obtained from 15 different countries. Our results demonstrate that while highly diverse, no new AGF genera were identified in the rumen mycobiome samples examined. Our analysis also indicate that animal host phylogeny, diet, biogeography, and domestication status could play a role in shaping AGF community structure. Finally, we demonstrate that a greater level of diversity and higher inter-sample variability was observed in rumen compared to fecal samples, with two genera (
and
) present in higher abundance in rumen samples, and two others (
and
) enriched in fecal samples. Our results provide a global view of the identity, diversity, and community structure of AGF in ruminants, elucidate factors impacting diversity and community structure of the rumen mycobiome, and identify patterns of AGF community variability between the rumen and feces in the herbivorous GI tract.</description><subject>Abundance</subject><subject>Anaerobic processes</subject><subject>Anaerobiosis</subject><subject>Animal species</subject><subject>Animals</subject><subject>Biogeography</subject><subject>Caecomyces</subject><subject>Community structure</subject><subject>Comparative analysis</subject><subject>Composition</subject><subject>Cyllamyces</subject><subject>Deer</subject><subject>Digestion</subject><subject>Digestive system</subject><subject>Domestication</subject><subject>Ecology</subject><subject>Feces</subject><subject>Fungi</subject><subject>Fungi - genetics</subject><subject>Gastrointestinal tract</subject><subject>Herbivores</subject><subject>Herbivory</subject><subject>Humans</subject><subject>Intestinal microflora</subject><subject>Microbial Ecology</subject><subject>Neocallimastix</subject><subject>Orpinomyces</subject><subject>Pattern analysis</subject><subject>Piromyces</subject><subject>Relative abundance</subject><subject>Rumen</subject><subject>Rumen - microbiology</subject><subject>Ruminants</subject><subject>Spotlight Selection</subject><subject>Structural analysis</subject><subject>Variability</subject><issn>0099-2240</issn><issn>1098-5336</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUtrFTEYhoMo9ljduZYBNxWc-uUy5yQrKfVWKLjRdcgk35yTMjOpuRzpvzfTU-sFugof78NDXl5CXlI4pZTJdwanU6BCsZbxR2RFQcm243z9mKwAlGoZE3BEnqV0BQAC1vIpOeKSKSUpXxH_we8xJp9vGjO7xoZpKvNypRyLzSViE4YaGYyh97bZltwMZd76xs9N3mETy4Tzwvz0o7t1uDBhyt6ajK7ZYez9PkRMz8mTwYwJX9y9x-T7p4_fzr-0l18_X5yfXbZGgMitk53qNo52g-MAHbPoKLdK2V4YwSg3HBm4fuCSComuRgYWUAACbJzjx-T9wXtd-gmdxTlHM-rr6CcTb3QwXv-bzH6nt2GvKUgJayar4eTOEMOPUrvoySeL42hmDCVpphilVEK3rujr_9CrUOJc-1WKb6QUG7lQbw-UjSGliMP9byjoZURdR9S3I2rGK_7mgJs0sT_CB9hXf7e9F_9emP8CHmSmYg</recordid><startdate>20240221</startdate><enddate>20240221</enddate><creator>Meili, Casey H</creator><creator>TagElDein, Moustafa A</creator><creator>Jones, Adrienne L</creator><creator>Moon, Christina D</creator><creator>Andrews, Catherine</creator><creator>Kirk, Michelle R</creator><creator>Janssen, Peter H</creator><creator>J Yeoman, Carl</creator><creator>Grace, Savannah</creator><creator>Borgogna, Joanna-Lynn C</creator><creator>Foote, Andrew P</creator><creator>Nagy, Yosra I</creator><creator>Kashef, Mona T</creator><creator>Yassin, Aymen S</creator><creator>Elshahed, Mostafa S</creator><creator>Youssef, Noha H</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>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1022-3502</orcidid><orcidid>https://orcid.org/0000-0003-0379-3440</orcidid><orcidid>https://orcid.org/0000-0002-4488-4042</orcidid><orcidid>https://orcid.org/0000-0001-9159-3785</orcidid><orcidid>https://orcid.org/0000-0001-9692-9559</orcidid></search><sort><creationdate>20240221</creationdate><title>Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores</title><author>Meili, Casey H ; TagElDein, Moustafa A ; Jones, Adrienne L ; Moon, Christina D ; Andrews, Catherine ; Kirk, Michelle R ; Janssen, Peter H ; J Yeoman, Carl ; Grace, Savannah ; Borgogna, Joanna-Lynn C ; Foote, Andrew P ; Nagy, Yosra I ; Kashef, Mona T ; Yassin, Aymen S ; Elshahed, Mostafa S ; Youssef, Noha H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a404t-d85957d15fd30052ced13c99cb4a4213a3e20dbf38148ed3c9a0300540e007dd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Abundance</topic><topic>Anaerobic processes</topic><topic>Anaerobiosis</topic><topic>Animal species</topic><topic>Animals</topic><topic>Biogeography</topic><topic>Caecomyces</topic><topic>Community structure</topic><topic>Comparative analysis</topic><topic>Composition</topic><topic>Cyllamyces</topic><topic>Deer</topic><topic>Digestion</topic><topic>Digestive system</topic><topic>Domestication</topic><topic>Ecology</topic><topic>Feces</topic><topic>Fungi</topic><topic>Fungi - genetics</topic><topic>Gastrointestinal tract</topic><topic>Herbivores</topic><topic>Herbivory</topic><topic>Humans</topic><topic>Intestinal microflora</topic><topic>Microbial Ecology</topic><topic>Neocallimastix</topic><topic>Orpinomyces</topic><topic>Pattern analysis</topic><topic>Piromyces</topic><topic>Relative abundance</topic><topic>Rumen</topic><topic>Rumen - microbiology</topic><topic>Ruminants</topic><topic>Spotlight Selection</topic><topic>Structural analysis</topic><topic>Variability</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Meili, Casey H</creatorcontrib><creatorcontrib>TagElDein, Moustafa A</creatorcontrib><creatorcontrib>Jones, Adrienne L</creatorcontrib><creatorcontrib>Moon, Christina D</creatorcontrib><creatorcontrib>Andrews, Catherine</creatorcontrib><creatorcontrib>Kirk, Michelle R</creatorcontrib><creatorcontrib>Janssen, Peter H</creatorcontrib><creatorcontrib>J Yeoman, Carl</creatorcontrib><creatorcontrib>Grace, Savannah</creatorcontrib><creatorcontrib>Borgogna, Joanna-Lynn C</creatorcontrib><creatorcontrib>Foote, Andrew P</creatorcontrib><creatorcontrib>Nagy, Yosra I</creatorcontrib><creatorcontrib>Kashef, Mona T</creatorcontrib><creatorcontrib>Yassin, Aymen S</creatorcontrib><creatorcontrib>Elshahed, Mostafa S</creatorcontrib><creatorcontrib>Youssef, Noha H</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Meili, Casey H</au><au>TagElDein, Moustafa A</au><au>Jones, Adrienne L</au><au>Moon, Christina D</au><au>Andrews, Catherine</au><au>Kirk, Michelle R</au><au>Janssen, Peter H</au><au>J Yeoman, Carl</au><au>Grace, Savannah</au><au>Borgogna, Joanna-Lynn C</au><au>Foote, Andrew P</au><au>Nagy, Yosra I</au><au>Kashef, Mona T</au><au>Yassin, Aymen S</au><au>Elshahed, Mostafa S</au><au>Youssef, Noha H</au><au>Reguera, Gemma</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores</atitle><jtitle>Applied and environmental microbiology</jtitle><stitle>Appl Environ Microbiol</stitle><addtitle>Appl Environ Microbiol</addtitle><date>2024-02-21</date><risdate>2024</risdate><volume>90</volume><issue>2</issue><spage>e0149223</spage><pages>e0149223-</pages><issn>0099-2240</issn><issn>1098-5336</issn><eissn>1098-5336</eissn><abstract>The rumen houses a diverse community that plays a major role in the digestion process in ruminants. Anaerobic gut fungi (AGF) are key contributors to plant digestion in the rumen. Here, we present a global amplicon-based survey of the rumen AGF mycobiome by examining 206 samples from 15 animal species, 15 countries, and 6 continents. The rumen AGF mycobiome was highly diverse, with 81 out of 88 currently recognized AGF genera or candidate genera identified. However, only six genera (
NY9, and
) were present at >4% relative abundance. AGF diversity was higher in members of the families
and
compared to
. Community structure analysis identified a pattern of phylosymbiosis, where host family (10% of total variance) and species (13.5%) partially explained the rumen mycobiome composition. As well, diet composition (9%-19%), domestication (11.14%), and biogeography (14.1%) also partially explained AGF community structure; although sampling limitation, geographic range restrictions, and direct association between different factors hindered accurate elucidation of the relative contribution of each factor. Pairwise comparison of rumen and fecal samples obtained from the same subject (
= 13) demonstrated greater diversity and inter-sample variability in rumen versus fecal samples. The genera
and
were present in higher abundance in rumen samples, while
and
were enriched in fecal samples. Comparative analysis of global rumen and feces data sets revealed a similar pattern. Our results provide a global view of AGF community in the rumen and identify patterns of AGF variability between rumen and feces in herbivores Gastrointestinal (GI) tract.IMPORTANCERuminants are highly successful and economically important mammalian suborder. Ruminants are herbivores that digest plant material with the aid of microorganisms residing in their GI tract. In ruminants, the rumen compartment represents the most important location where microbially mediated plant digestion occurs, and is known to house a bewildering array of microbial diversity. An important component of the rumen microbiome is the anaerobic gut fungi (AGF), members of the phylum
. So far, studies examining AGF diversity have mostly employed fecal samples, and little is currently known regarding the identity of AGF residing in the rumen compartment, factors that impact the observed patterns of diversity and community structure of AGF in the rumen, and how AGF communities in the rumen compare to AGF communities in feces. Here, we examined the rumen AGF diversity using an amplicon-based survey targeting a wide range of wild and domesticated ruminants (
= 206, 15 different animal species) obtained from 15 different countries. Our results demonstrate that while highly diverse, no new AGF genera were identified in the rumen mycobiome samples examined. Our analysis also indicate that animal host phylogeny, diet, biogeography, and domestication status could play a role in shaping AGF community structure. Finally, we demonstrate that a greater level of diversity and higher inter-sample variability was observed in rumen compared to fecal samples, with two genera (
and
) present in higher abundance in rumen samples, and two others (
and
) enriched in fecal samples. Our results provide a global view of the identity, diversity, and community structure of AGF in ruminants, elucidate factors impacting diversity and community structure of the rumen mycobiome, and identify patterns of AGF community variability between the rumen and feces in the herbivorous GI tract.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>38299813</pmid><doi>10.1128/aem.01492-23</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-1022-3502</orcidid><orcidid>https://orcid.org/0000-0003-0379-3440</orcidid><orcidid>https://orcid.org/0000-0002-4488-4042</orcidid><orcidid>https://orcid.org/0000-0001-9159-3785</orcidid><orcidid>https://orcid.org/0000-0001-9692-9559</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0099-2240 |
| ispartof | Applied and environmental microbiology, 2024-02, Vol.90 (2), p.e0149223 |
| issn | 0099-2240 1098-5336 1098-5336 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10880628 |
| source | MEDLINE; American Society for Microbiology Journals; PubMed Central; Alma/SFX Local Collection |
| subjects | Abundance Anaerobic processes Anaerobiosis Animal species Animals Biogeography Caecomyces Community structure Comparative analysis Composition Cyllamyces Deer Digestion Digestive system Domestication Ecology Feces Fungi Fungi - genetics Gastrointestinal tract Herbivores Herbivory Humans Intestinal microflora Microbial Ecology Neocallimastix Orpinomyces Pattern analysis Piromyces Relative abundance Rumen Rumen - microbiology Ruminants Spotlight Selection Structural analysis Variability |
| title | Diversity and community structure of anaerobic gut fungi in the rumen of wild and domesticated herbivores |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-04T15%3A47%3A56IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Diversity%20and%20community%20structure%20of%20anaerobic%20gut%20fungi%20in%20the%20rumen%20of%20wild%20and%20domesticated%20herbivores&rft.jtitle=Applied%20and%20environmental%20microbiology&rft.au=Meili,%20Casey%20H&rft.date=2024-02-21&rft.volume=90&rft.issue=2&rft.spage=e0149223&rft.pages=e0149223-&rft.issn=0099-2240&rft.eissn=1098-5336&rft_id=info:doi/10.1128/aem.01492-23&rft_dat=%3Cproquest_pubme%3E2921118056%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2937884786&rft_id=info:pmid/38299813&rfr_iscdi=true |