Genomic insights into the evolution of secondary metabolism of Escovopsis and its allies, specialized fungal symbionts of fungus-farming ants

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Autor(es): dc.contributorEmory University-
Autor(es): dc.contributorUniversity of Tübingen-
Autor(es): dc.contributorMax Planck Institute for Biology-
Autor(es): dc.contributorVrije Universiteit Amsterdam-
Autor(es): dc.contributorEmory University School of Medicine-
Autor(es): dc.contributorInstituto de Investigaciones Científicas y Servicios de Alta Tecnología-
Autor(es): dc.contributorUniversidade Estadual Paulista (UNESP)-
Autor(es): dc.contributorBerry College-
Autor(es): dc.creatorBerasategui, Aileen-
Autor(es): dc.creatorSalem, Hassan-
Autor(es): dc.creatorMoller, Abraham G.-
Autor(es): dc.creatorChristopher, Yuliana-
Autor(es): dc.creatorMontoya, Quimi Vidaurre-
Autor(es): dc.creatorConn, Caitlin-
Autor(es): dc.creatorRead, Timothy D.-
Autor(es): dc.creatorRodrigues, Andre-
Autor(es): dc.creatorZiemert, Nadine-
Autor(es): dc.creatorGerardo, Nicole-
Data de aceite: dc.date.accessioned2025-08-21T15:36:38Z-
Data de disponibilização: dc.date.available2025-08-21T15:36:38Z-
Data de envio: dc.date.issued2025-04-29-
Data de envio: dc.date.issued2024-07-01-
Fonte completa do material: dc.identifierhttp://dx.doi.org/10.1128/msystems.00576-24-
Fonte completa do material: dc.identifierhttps://hdl.handle.net/11449/297284-
Fonte: dc.identifier.urihttp://educapes.capes.gov.br/handle/11449/297284-
Descrição: dc.descriptionThe metabolic intimacy of symbiosis often demands the work of specialists. Natural products and defensive secondary metabolites can drive specificity by ensuring infection and propagation across host generations. But in contrast to bacteria, little is known about the diversity and distribution of natural product biosynthetic pathways among fungi and how they evolve to facilitate symbiosis and adaptation to their host environment. In this study, we define the secondary metabolism of Escovopsis and closely related genera, symbionts in the gardens of fungus-farming ants. We ask how the gain and loss of various biosynthetic pathways correspond to divergent lifestyles. Long-read sequencing allowed us to define the chromosomal features of representative Escovopsis strains, revealing highly reduced genomes composed of seven to eight chromosomes. The genomes are highly syntenic with macrosynteny decreasing with increasing phylogenetic distance, while maintaining a high degree of mesosynteny. An ancestral state reconstruction analysis of biosynthetic pathways revealed that, while many secondary metabolites are shared with non-ant-associated Sordariomycetes, 56 pathways are unique to the symbiotic genera. Reflecting adaptation to diverging ant agricultural systems, we observe that the stepwise acquisition of these pathways mirrors the ecological radiations of attine ants and the dynamic recruitment and replacement of their fungal cultivars. As different clades encode characteristic combinations of biosynthetic gene clusters, these delineating profiles provide important insights into the possible mechanisms underlying specificity between these symbionts and their fungal hosts. Collectively, our findings shed light on the evolutionary dynamic nature of secondary metabolism in Escovopsis and its allies, reflecting adaptation of the symbionts to an ancient agricultural system. IMPORTANCE Microbial symbionts interact with their hosts and competitors through a remarkable array of secondary metabolites and natural products. Here, we highlight the highly streamlined genomic features of attine-associated fungal symbionts. The genomes of Escovopsis species, as well as species from other symbiont genera, many of which are common with the gardens of fungus-growing ants, are defined by seven chromosomes. Despite a high degree of metabolic conservation, we observe some variation in the symbionts’ potential to produce secondary metabolites. As the phylogenetic distribution of the encoding biosynthetic gene clusters coincides with attine transitions in agricultural systems, we highlight the likely role of these metabolites in mediating adaptation by a group of highly specialized symbionts.-
Descrição: dc.descriptionAlexander von Humboldt-Stiftung-
Descrição: dc.descriptionNational Science Foundation-
Descrição: dc.descriptionFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)-
Descrição: dc.descriptionDeutsche Forschungsgemeinschaft-
Descrição: dc.descriptionNational Natural Science Foundation of China-
Descrição: dc.descriptionDepartment of Biology Emory University-
Descrição: dc.descriptionCluster of Excellence-Controlling Microbes to Fight Infections University of Tübingen-
Descrição: dc.descriptionMutualisms Research Group Max Planck Institute for Biology-
Descrição: dc.descriptionAmsterdam Institute for Life and Environment Vrije Universiteit Amsterdam-
Descrição: dc.descriptionDivision of Infectious Diseases Emory University School of Medicine-
Descrição: dc.descriptionInstituto de Investigaciones Científicas y Servicios de Alta Tecnología, Ciudad del Saber-
Descrição: dc.descriptionDepartment of General and Applied Biology São Paulo State University (UNESP) Institute of Biosciences, Rio Claro-
Descrição: dc.descriptionDepartment of Biology Berry College-
Descrição: dc.descriptionTranslational Genome Mining for Natural Products Interfaculty Institute of Microbiology and Infection Medicine Tübingen (IMIT) Interfaculty Institute for Biomedical Informatics (IBMI) University of Tübingen-
Descrição: dc.descriptionDepartment of General and Applied Biology São Paulo State University (UNESP) Institute of Biosciences, Rio Claro-
Descrição: dc.descriptionNational Science Foundation: 1711545-
Descrição: dc.descriptionNational Science Foundation: 1754595-
Descrição: dc.descriptionNational Science Foundation: 1927411-
Descrição: dc.descriptionFAPESP: 2019/03746-0-
Descrição: dc.descriptionFAPESP: 2019/03746-0 and 2021/04706-1-
Descrição: dc.descriptionFAPESP: 2021/04706-1-
Descrição: dc.descriptionDeutsche Forschungsgemeinschaft: BE6922/1-1-
Descrição: dc.descriptionNational Natural Science Foundation of China: DBI-711545-
Descrição: dc.descriptionNational Natural Science Foundation of China: DEB-1754595-
Descrição: dc.descriptionNational Natural Science Foundation of China: DEB-1927411-
Descrição: dc.descriptionDeutsche Forschungsgemeinschaft: EXC 2124 - 390838134-
Idioma: dc.languageen-
Relação: dc.relationmSystems-
???dc.source???: dc.sourceScopus-
Palavras-chave: dc.subjectparasitism-
Palavras-chave: dc.subjectsecondary metabolism-
Palavras-chave: dc.subjectsymbiosis-
Título: dc.titleGenomic insights into the evolution of secondary metabolism of Escovopsis and its allies, specialized fungal symbionts of fungus-farming ants-
Tipo de arquivo: dc.typelivro digital-
Aparece nas coleções:Repositório Institucional - Unesp

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