Patterns and determinants of the global herbivorous mycobiome

Autores
Meili, Markus; Jones, Adriane; Arreola, Alex; Habel, Jeffrey; Pratt, Carrie; Hanafy, Radwa; Wang, Yan; Yassin, Aymen; TagElDein, Moustafa; Moon, Christina; Janssen, Peter; Shrestha, Mitesh; Rajbhandari, Prajwal; Nagler, Magdalena; Vinzelj, Julia; Podmirseg, Sabine; Stajich, Jason; Goetsch, Arthur; Hayes, Jerry; Young, Diana; Fliegerova, Katerine; Grilli, Diego Javier; Vodička, Roman; Moniello, Giusepe; Mattiello, Silvana; Kashef, Mona; Nagy, Yosra; Edwards, Joan A.; Singh Dagar, Sumit; Foote, Andrew; Youssef, Noha; Elshahed, Mostafa
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In spite of their indispensable role in host nutrition, the anaerobic gut fungal (AGF) component of the herbivorous gut microbiome remains poorly characterized. To examine global patterns and determinants of AGF diversity, we generated and analyzed an amplicon dataset from 661 fecal samples from 34 animal species, 9 families, and 6 continents. We identified novel genera, greatly expanding AGF diversity beyond current estimates. Both stochastic (homogenizing dispersal and drift) and deterministic (homogenizing selection) processes played an integral role in shaping AGF communities, with a higher level of stochasticity observed in foregut fermenters. Community structure analysis revealed a distinct pattern of phylosymbiosis, where host-associated (animal species, family, and gut type), rather than ecological (domestication status and biogeography) factors predominantly shaped the community. Hindgut fermenters exhibited stronger and more specific fungal-host associations, compared to broader mostly non-host specific associations in foregut fermenters. Transcriptomics-enabled phylogenomic and molecular clock analyses of 52 strains from 14 genera indicated that most genera with preferences for hindgut hosts evolved earlier (44-58 Mya), while those with preferences for foregut hosts evolved more recently (22-32 Mya). This pattern is in agreement with the sole dependence of herbivores on hindgut fermentation past the Cretaceous-Paleogene (K-Pg) extinction event through the Paleocene and Eocene, and the later rapid evolution of animals employing foregut fermentation strategy during the early Miocene. Only a few AGF genera deviated from this pattern of co-evolutionary phylosymbiosis, by exhibiting preferences suggestive of post-evolutionary environmental filtering. Our results greatly expand the documented scope of AGF diversity and provide an ecologically and evolutionary-grounded model to explain the observed patterns of AGF diversity in extant animal hosts.
Fil: Meili, Markus. Oklahoma State University; Estados Unidos
Fil: Jones, Adriane. Oklahoma State University; Estados Unidos
Fil: Arreola, Alex. Oklahoma State University; Estados Unidos
Fil: Habel, Jeffrey. Oklahoma State University; Estados Unidos
Fil: Pratt, Carrie. Oklahoma State University; Estados Unidos
Fil: Hanafy, Radwa. Oklahoma State University; Estados Unidos
Fil: Wang, Yan. University of Toronto; Canadá
Fil: Yassin, Aymen. Cairo University; Egipto
Fil: TagElDein, Moustafa. Cairo University; Egipto
Fil: Moon, Christina. Grasslands Research Centre. Agresearch Limited; Nueva Zelanda
Fil: Janssen, Peter. Grasslands Research Centre. Agresearch Limited; Nueva Zelanda
Fil: Shrestha, Mitesh. Research Institute For Bioscience And Biotechnology; Nepal
Fil: Rajbhandari, Prajwal. Research Institute For Bioscience And Biotechnology; Nepal
Fil: Nagler, Magdalena. Universidad de Innsbruck; Austria
Fil: Vinzelj, Julia. Universidad de Innsbruck; Austria
Fil: Podmirseg, Sabine. Universidad de Innsbruck; Austria
Fil: Stajich, Jason. University of California; Estados Unidos
Fil: Goetsch, Arthur. Langston University; Estados Unidos
Fil: Hayes, Jerry. Langston University; Estados Unidos
Fil: Young, Diana. Bavarian State Research Center For Agriculture; Alemania
Fil: Fliegerova, Katerine. Czech Academy of Sciences; República Checa
Fil: Grilli, Diego Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza; Argentina. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas; Argentina
Fil: Vodička, Roman. Prague Zoo; República Checa
Fil: Moniello, Giusepe. University Of Sassari; Italia
Fil: Mattiello, Silvana. Università degli Studi di Milano; Italia
Fil: Kashef, Mona. Cairo University; Egipto
Fil: Nagy, Yosra. Cairo University; Egipto
Fil: Edwards, Joan A.. Anaerobic Fungi Network; Países Bajos
Fil: Singh Dagar, Sumit. Agharkar Research Institute; India
Fil: Foote, Andrew. Oklahoma State University; Estados Unidos
Fil: Youssef, Noha. Oklahoma State University; Estados Unidos
Fil: Elshahed, Mostafa. Oklahoma State University; Estados Unidos
Materia
MICROBIOTA
MYCOBIOMA
GUT
HERBIVOROUS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/233939

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spelling Patterns and determinants of the global herbivorous mycobiomeMeili, MarkusJones, AdrianeArreola, AlexHabel, JeffreyPratt, CarrieHanafy, RadwaWang, YanYassin, AymenTagElDein, MoustafaMoon, ChristinaJanssen, PeterShrestha, MiteshRajbhandari, PrajwalNagler, MagdalenaVinzelj, JuliaPodmirseg, SabineStajich, JasonGoetsch, ArthurHayes, JerryYoung, DianaFliegerova, KaterineGrilli, Diego JavierVodička, RomanMoniello, GiusepeMattiello, SilvanaKashef, MonaNagy, YosraEdwards, Joan A.Singh Dagar, SumitFoote, AndrewYoussef, NohaElshahed, MostafaMICROBIOTAMYCOBIOMAGUTHERBIVOROUShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1In spite of their indispensable role in host nutrition, the anaerobic gut fungal (AGF) component of the herbivorous gut microbiome remains poorly characterized. To examine global patterns and determinants of AGF diversity, we generated and analyzed an amplicon dataset from 661 fecal samples from 34 animal species, 9 families, and 6 continents. We identified novel genera, greatly expanding AGF diversity beyond current estimates. Both stochastic (homogenizing dispersal and drift) and deterministic (homogenizing selection) processes played an integral role in shaping AGF communities, with a higher level of stochasticity observed in foregut fermenters. Community structure analysis revealed a distinct pattern of phylosymbiosis, where host-associated (animal species, family, and gut type), rather than ecological (domestication status and biogeography) factors predominantly shaped the community. Hindgut fermenters exhibited stronger and more specific fungal-host associations, compared to broader mostly non-host specific associations in foregut fermenters. Transcriptomics-enabled phylogenomic and molecular clock analyses of 52 strains from 14 genera indicated that most genera with preferences for hindgut hosts evolved earlier (44-58 Mya), while those with preferences for foregut hosts evolved more recently (22-32 Mya). This pattern is in agreement with the sole dependence of herbivores on hindgut fermentation past the Cretaceous-Paleogene (K-Pg) extinction event through the Paleocene and Eocene, and the later rapid evolution of animals employing foregut fermentation strategy during the early Miocene. Only a few AGF genera deviated from this pattern of co-evolutionary phylosymbiosis, by exhibiting preferences suggestive of post-evolutionary environmental filtering. Our results greatly expand the documented scope of AGF diversity and provide an ecologically and evolutionary-grounded model to explain the observed patterns of AGF diversity in extant animal hosts.Fil: Meili, Markus. Oklahoma State University; Estados UnidosFil: Jones, Adriane. Oklahoma State University; Estados UnidosFil: Arreola, Alex. Oklahoma State University; Estados UnidosFil: Habel, Jeffrey. Oklahoma State University; Estados UnidosFil: Pratt, Carrie. Oklahoma State University; Estados UnidosFil: Hanafy, Radwa. Oklahoma State University; Estados UnidosFil: Wang, Yan. University of Toronto; CanadáFil: Yassin, Aymen. Cairo University; EgiptoFil: TagElDein, Moustafa. Cairo University; EgiptoFil: Moon, Christina. Grasslands Research Centre. Agresearch Limited; Nueva ZelandaFil: Janssen, Peter. Grasslands Research Centre. Agresearch Limited; Nueva ZelandaFil: Shrestha, Mitesh. Research Institute For Bioscience And Biotechnology; NepalFil: Rajbhandari, Prajwal. Research Institute For Bioscience And Biotechnology; NepalFil: Nagler, Magdalena. Universidad de Innsbruck; AustriaFil: Vinzelj, Julia. Universidad de Innsbruck; AustriaFil: Podmirseg, Sabine. Universidad de Innsbruck; AustriaFil: Stajich, Jason. University of California; Estados UnidosFil: Goetsch, Arthur. Langston University; Estados UnidosFil: Hayes, Jerry. Langston University; Estados UnidosFil: Young, Diana. Bavarian State Research Center For Agriculture; AlemaniaFil: Fliegerova, Katerine. Czech Academy of Sciences; República ChecaFil: Grilli, Diego Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza; Argentina. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas; ArgentinaFil: Vodička, Roman. Prague Zoo; República ChecaFil: Moniello, Giusepe. University Of Sassari; ItaliaFil: Mattiello, Silvana. Università degli Studi di Milano; ItaliaFil: Kashef, Mona. Cairo University; EgiptoFil: Nagy, Yosra. Cairo University; EgiptoFil: Edwards, Joan A.. Anaerobic Fungi Network; Países BajosFil: Singh Dagar, Sumit. Agharkar Research Institute; IndiaFil: Foote, Andrew. Oklahoma State University; Estados UnidosFil: Youssef, Noha. Oklahoma State University; Estados UnidosFil: Elshahed, Mostafa. Oklahoma State University; Estados UnidosSpringer2023-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/233939Meili, Markus; Jones, Adriane; Arreola, Alex; Habel, Jeffrey; Pratt, Carrie; et al.; Patterns and determinants of the global herbivorous mycobiome; Springer; Nature Communications; 14; 1; 6-2023; 1-182041-1723CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41467-023-39508-zinfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41467-023-39508-zinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:33:19Zoai:ri.conicet.gov.ar:11336/233939instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:33:19.999CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Patterns and determinants of the global herbivorous mycobiome
title Patterns and determinants of the global herbivorous mycobiome
spellingShingle Patterns and determinants of the global herbivorous mycobiome
Meili, Markus
MICROBIOTA
MYCOBIOMA
GUT
HERBIVOROUS
title_short Patterns and determinants of the global herbivorous mycobiome
title_full Patterns and determinants of the global herbivorous mycobiome
title_fullStr Patterns and determinants of the global herbivorous mycobiome
title_full_unstemmed Patterns and determinants of the global herbivorous mycobiome
title_sort Patterns and determinants of the global herbivorous mycobiome
dc.creator.none.fl_str_mv Meili, Markus
Jones, Adriane
Arreola, Alex
Habel, Jeffrey
Pratt, Carrie
Hanafy, Radwa
Wang, Yan
Yassin, Aymen
TagElDein, Moustafa
Moon, Christina
Janssen, Peter
Shrestha, Mitesh
Rajbhandari, Prajwal
Nagler, Magdalena
Vinzelj, Julia
Podmirseg, Sabine
Stajich, Jason
Goetsch, Arthur
Hayes, Jerry
Young, Diana
Fliegerova, Katerine
Grilli, Diego Javier
Vodička, Roman
Moniello, Giusepe
Mattiello, Silvana
Kashef, Mona
Nagy, Yosra
Edwards, Joan A.
Singh Dagar, Sumit
Foote, Andrew
Youssef, Noha
Elshahed, Mostafa
author Meili, Markus
author_facet Meili, Markus
Jones, Adriane
Arreola, Alex
Habel, Jeffrey
Pratt, Carrie
Hanafy, Radwa
Wang, Yan
Yassin, Aymen
TagElDein, Moustafa
Moon, Christina
Janssen, Peter
Shrestha, Mitesh
Rajbhandari, Prajwal
Nagler, Magdalena
Vinzelj, Julia
Podmirseg, Sabine
Stajich, Jason
Goetsch, Arthur
Hayes, Jerry
Young, Diana
Fliegerova, Katerine
Grilli, Diego Javier
Vodička, Roman
Moniello, Giusepe
Mattiello, Silvana
Kashef, Mona
Nagy, Yosra
Edwards, Joan A.
Singh Dagar, Sumit
Foote, Andrew
Youssef, Noha
Elshahed, Mostafa
author_role author
author2 Jones, Adriane
Arreola, Alex
Habel, Jeffrey
Pratt, Carrie
Hanafy, Radwa
Wang, Yan
Yassin, Aymen
TagElDein, Moustafa
Moon, Christina
Janssen, Peter
Shrestha, Mitesh
Rajbhandari, Prajwal
Nagler, Magdalena
Vinzelj, Julia
Podmirseg, Sabine
Stajich, Jason
Goetsch, Arthur
Hayes, Jerry
Young, Diana
Fliegerova, Katerine
Grilli, Diego Javier
Vodička, Roman
Moniello, Giusepe
Mattiello, Silvana
Kashef, Mona
Nagy, Yosra
Edwards, Joan A.
Singh Dagar, Sumit
Foote, Andrew
Youssef, Noha
Elshahed, Mostafa
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv MICROBIOTA
MYCOBIOMA
GUT
HERBIVOROUS
topic MICROBIOTA
MYCOBIOMA
GUT
HERBIVOROUS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv In spite of their indispensable role in host nutrition, the anaerobic gut fungal (AGF) component of the herbivorous gut microbiome remains poorly characterized. To examine global patterns and determinants of AGF diversity, we generated and analyzed an amplicon dataset from 661 fecal samples from 34 animal species, 9 families, and 6 continents. We identified novel genera, greatly expanding AGF diversity beyond current estimates. Both stochastic (homogenizing dispersal and drift) and deterministic (homogenizing selection) processes played an integral role in shaping AGF communities, with a higher level of stochasticity observed in foregut fermenters. Community structure analysis revealed a distinct pattern of phylosymbiosis, where host-associated (animal species, family, and gut type), rather than ecological (domestication status and biogeography) factors predominantly shaped the community. Hindgut fermenters exhibited stronger and more specific fungal-host associations, compared to broader mostly non-host specific associations in foregut fermenters. Transcriptomics-enabled phylogenomic and molecular clock analyses of 52 strains from 14 genera indicated that most genera with preferences for hindgut hosts evolved earlier (44-58 Mya), while those with preferences for foregut hosts evolved more recently (22-32 Mya). This pattern is in agreement with the sole dependence of herbivores on hindgut fermentation past the Cretaceous-Paleogene (K-Pg) extinction event through the Paleocene and Eocene, and the later rapid evolution of animals employing foregut fermentation strategy during the early Miocene. Only a few AGF genera deviated from this pattern of co-evolutionary phylosymbiosis, by exhibiting preferences suggestive of post-evolutionary environmental filtering. Our results greatly expand the documented scope of AGF diversity and provide an ecologically and evolutionary-grounded model to explain the observed patterns of AGF diversity in extant animal hosts.
Fil: Meili, Markus. Oklahoma State University; Estados Unidos
Fil: Jones, Adriane. Oklahoma State University; Estados Unidos
Fil: Arreola, Alex. Oklahoma State University; Estados Unidos
Fil: Habel, Jeffrey. Oklahoma State University; Estados Unidos
Fil: Pratt, Carrie. Oklahoma State University; Estados Unidos
Fil: Hanafy, Radwa. Oklahoma State University; Estados Unidos
Fil: Wang, Yan. University of Toronto; Canadá
Fil: Yassin, Aymen. Cairo University; Egipto
Fil: TagElDein, Moustafa. Cairo University; Egipto
Fil: Moon, Christina. Grasslands Research Centre. Agresearch Limited; Nueva Zelanda
Fil: Janssen, Peter. Grasslands Research Centre. Agresearch Limited; Nueva Zelanda
Fil: Shrestha, Mitesh. Research Institute For Bioscience And Biotechnology; Nepal
Fil: Rajbhandari, Prajwal. Research Institute For Bioscience And Biotechnology; Nepal
Fil: Nagler, Magdalena. Universidad de Innsbruck; Austria
Fil: Vinzelj, Julia. Universidad de Innsbruck; Austria
Fil: Podmirseg, Sabine. Universidad de Innsbruck; Austria
Fil: Stajich, Jason. University of California; Estados Unidos
Fil: Goetsch, Arthur. Langston University; Estados Unidos
Fil: Hayes, Jerry. Langston University; Estados Unidos
Fil: Young, Diana. Bavarian State Research Center For Agriculture; Alemania
Fil: Fliegerova, Katerine. Czech Academy of Sciences; República Checa
Fil: Grilli, Diego Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza; Argentina. Universidad Nacional de Cuyo. Facultad de Ciencias Médicas; Argentina
Fil: Vodička, Roman. Prague Zoo; República Checa
Fil: Moniello, Giusepe. University Of Sassari; Italia
Fil: Mattiello, Silvana. Università degli Studi di Milano; Italia
Fil: Kashef, Mona. Cairo University; Egipto
Fil: Nagy, Yosra. Cairo University; Egipto
Fil: Edwards, Joan A.. Anaerobic Fungi Network; Países Bajos
Fil: Singh Dagar, Sumit. Agharkar Research Institute; India
Fil: Foote, Andrew. Oklahoma State University; Estados Unidos
Fil: Youssef, Noha. Oklahoma State University; Estados Unidos
Fil: Elshahed, Mostafa. Oklahoma State University; Estados Unidos
description In spite of their indispensable role in host nutrition, the anaerobic gut fungal (AGF) component of the herbivorous gut microbiome remains poorly characterized. To examine global patterns and determinants of AGF diversity, we generated and analyzed an amplicon dataset from 661 fecal samples from 34 animal species, 9 families, and 6 continents. We identified novel genera, greatly expanding AGF diversity beyond current estimates. Both stochastic (homogenizing dispersal and drift) and deterministic (homogenizing selection) processes played an integral role in shaping AGF communities, with a higher level of stochasticity observed in foregut fermenters. Community structure analysis revealed a distinct pattern of phylosymbiosis, where host-associated (animal species, family, and gut type), rather than ecological (domestication status and biogeography) factors predominantly shaped the community. Hindgut fermenters exhibited stronger and more specific fungal-host associations, compared to broader mostly non-host specific associations in foregut fermenters. Transcriptomics-enabled phylogenomic and molecular clock analyses of 52 strains from 14 genera indicated that most genera with preferences for hindgut hosts evolved earlier (44-58 Mya), while those with preferences for foregut hosts evolved more recently (22-32 Mya). This pattern is in agreement with the sole dependence of herbivores on hindgut fermentation past the Cretaceous-Paleogene (K-Pg) extinction event through the Paleocene and Eocene, and the later rapid evolution of animals employing foregut fermentation strategy during the early Miocene. Only a few AGF genera deviated from this pattern of co-evolutionary phylosymbiosis, by exhibiting preferences suggestive of post-evolutionary environmental filtering. Our results greatly expand the documented scope of AGF diversity and provide an ecologically and evolutionary-grounded model to explain the observed patterns of AGF diversity in extant animal hosts.
publishDate 2023
dc.date.none.fl_str_mv 2023-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/233939
Meili, Markus; Jones, Adriane; Arreola, Alex; Habel, Jeffrey; Pratt, Carrie; et al.; Patterns and determinants of the global herbivorous mycobiome; Springer; Nature Communications; 14; 1; 6-2023; 1-18
2041-1723
CONICET Digital
CONICET
url http://hdl.handle.net/11336/233939
identifier_str_mv Meili, Markus; Jones, Adriane; Arreola, Alex; Habel, Jeffrey; Pratt, Carrie; et al.; Patterns and determinants of the global herbivorous mycobiome; Springer; Nature Communications; 14; 1; 6-2023; 1-18
2041-1723
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41467-023-39508-z
info:eu-repo/semantics/altIdentifier/doi/10.1038/s41467-023-39508-z
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Springer
publisher.none.fl_str_mv Springer
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repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
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