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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/233939
Ver los metadatos del registro completo
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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 |
dc.source.none.fl_str_mv |
reponame:CONICET Digital (CONICET) instname:Consejo Nacional de Investigaciones Científicas y Técnicas |
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Consejo Nacional de Investigaciones Científicas y Técnicas |
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CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas |
repository.mail.fl_str_mv |
dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar |
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13.070432 |