Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis

ABSTRACT Modern genomics has shed light on many entomopathogenic fungi and expanded our knowledge widely; however, little is known about the genomic features of the insect-commensal fungi. Harpellales are obligate commensals living in the digestive tracts of disease-bearing insects (black flies, mid...

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Autores principales:	Yan Wang, Matt Stata, Wei Wang, Jason E. Stajich, Merlin M. White, Jean-Marc Moncalvo
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	FISCoG phylogenomics Trichomycetes Zoopagomycota Zygomycota Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d723dcbea20149e69ef5ee7e83442d0d
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spelling	oai:doaj.org-article:d723dcbea20149e69ef5ee7e83442d0d2021-11-15T16:00:25ZComparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis10.1128/mBio.00636-182150-7511https://doaj.org/article/d723dcbea20149e69ef5ee7e83442d0d2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00636-18https://doaj.org/toc/2150-7511ABSTRACT Modern genomics has shed light on many entomopathogenic fungi and expanded our knowledge widely; however, little is known about the genomic features of the insect-commensal fungi. Harpellales are obligate commensals living in the digestive tracts of disease-bearing insects (black flies, midges, and mosquitoes). In this study, we produced and annotated whole-genome sequences of nine Harpellales taxa and conducted the first comparative analyses to infer the genomic diversity within the members of the Harpellales. The genomes of the insect gut fungi feature low (26% to 37%) GC content and large genome size variations (25 to 102 Mb). Further comparisons with insect-pathogenic fungi (from both Ascomycota and Zoopagomycota), as well as with free-living relatives (as negative controls), helped to identify a gene toolbox that is essential to the fungus-insect symbiosis. The results not only narrow the genomic scope of fungus-insect interactions from several thousands to eight core players but also distinguish host invasion strategies employed by insect pathogens and commensals. The genomic content suggests that insect commensal fungi rely mostly on adhesion protein anchors that target digestive system, while entomopathogenic fungi have higher numbers of transmembrane helices, signal peptides, and pathogen-host interaction (PHI) genes across the whole genome and enrich genes as well as functional domains to inactivate the host inflammation system and suppress the host defense. Phylogenomic analyses have revealed that genome sizes of Harpellales fungi vary among lineages with an integer-multiple pattern, which implies that ancient genome duplications may have occurred within the gut of insects. IMPORTANCE Insect guts harbor various microbes that are important for host digestion, immune response, and disease dispersal in certain cases. Bacteria, which are among the primary endosymbionts, have been studied extensively. However, fungi, which are also frequently encountered, are poorly known with respect to their biology within the insect guts. To understand the genomic features and related biology, we produced the whole-genome sequences of nine gut commensal fungi from disease-bearing insects (black flies, midges, and mosquitoes). The results show that insect gut fungi tend to have low GC content across their genomes. By comparing these commensals with entomopathogenic and free-living fungi that have available genome sequences, we found a universal core gene toolbox that is unique and thus potentially important for the insect-fungus symbiosis. This comparative work also uncovered different host invasion strategies employed by insect pathogens and commensals, as well as a model system to study ancient fungal genome duplication within the gut of insects.Yan WangMatt StataWei WangJason E. StajichMerlin M. WhiteJean-Marc MoncalvoAmerican Society for MicrobiologyarticleFISCoGphylogenomicsTrichomycetesZoopagomycotaZygomycotaMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	FISCoG phylogenomics Trichomycetes Zoopagomycota Zygomycota Microbiology QR1-502
spellingShingle	FISCoG phylogenomics Trichomycetes Zoopagomycota Zygomycota Microbiology QR1-502 Yan Wang Matt Stata Wei Wang Jason E. Stajich Merlin M. White Jean-Marc Moncalvo Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis
description	ABSTRACT Modern genomics has shed light on many entomopathogenic fungi and expanded our knowledge widely; however, little is known about the genomic features of the insect-commensal fungi. Harpellales are obligate commensals living in the digestive tracts of disease-bearing insects (black flies, midges, and mosquitoes). In this study, we produced and annotated whole-genome sequences of nine Harpellales taxa and conducted the first comparative analyses to infer the genomic diversity within the members of the Harpellales. The genomes of the insect gut fungi feature low (26% to 37%) GC content and large genome size variations (25 to 102 Mb). Further comparisons with insect-pathogenic fungi (from both Ascomycota and Zoopagomycota), as well as with free-living relatives (as negative controls), helped to identify a gene toolbox that is essential to the fungus-insect symbiosis. The results not only narrow the genomic scope of fungus-insect interactions from several thousands to eight core players but also distinguish host invasion strategies employed by insect pathogens and commensals. The genomic content suggests that insect commensal fungi rely mostly on adhesion protein anchors that target digestive system, while entomopathogenic fungi have higher numbers of transmembrane helices, signal peptides, and pathogen-host interaction (PHI) genes across the whole genome and enrich genes as well as functional domains to inactivate the host inflammation system and suppress the host defense. Phylogenomic analyses have revealed that genome sizes of Harpellales fungi vary among lineages with an integer-multiple pattern, which implies that ancient genome duplications may have occurred within the gut of insects. IMPORTANCE Insect guts harbor various microbes that are important for host digestion, immune response, and disease dispersal in certain cases. Bacteria, which are among the primary endosymbionts, have been studied extensively. However, fungi, which are also frequently encountered, are poorly known with respect to their biology within the insect guts. To understand the genomic features and related biology, we produced the whole-genome sequences of nine gut commensal fungi from disease-bearing insects (black flies, midges, and mosquitoes). The results show that insect gut fungi tend to have low GC content across their genomes. By comparing these commensals with entomopathogenic and free-living fungi that have available genome sequences, we found a universal core gene toolbox that is unique and thus potentially important for the insect-fungus symbiosis. This comparative work also uncovered different host invasion strategies employed by insect pathogens and commensals, as well as a model system to study ancient fungal genome duplication within the gut of insects.
format	article
author	Yan Wang Matt Stata Wei Wang Jason E. Stajich Merlin M. White Jean-Marc Moncalvo
author_facet	Yan Wang Matt Stata Wei Wang Jason E. Stajich Merlin M. White Jean-Marc Moncalvo
author_sort	Yan Wang
title	Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis
title_short	Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis
title_full	Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis
title_fullStr	Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis
title_full_unstemmed	Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis
title_sort	comparative genomics reveals the core gene toolbox for the fungus-insect symbiosis
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/d723dcbea20149e69ef5ee7e83442d0d
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Comparative Genomics Reveals the Core Gene Toolbox for the Fungus-Insect Symbiosis

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