Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

ABSTRACT Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome...

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Autores principales:	Karissa L. Cross, Brittany A. Leigh, E. Anne Hatmaker, Aram Mikaelyan, Asia K. Miller, Seth R. Bordenstein
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Proteus Providencia Nasonia gut bacteria microbiome phage Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/7921dd2690744498b5414e2eccba5c47
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spelling	oai:doaj.org-article:7921dd2690744498b5414e2eccba5c472021-12-02T19:22:27ZGenomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown10.1128/mSystems.01342-202379-5077https://doaj.org/article/7921dd2690744498b5414e2eccba5c472021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01342-20https://doaj.org/toc/2379-5077ABSTRACT Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacterium in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterium-assisted lethality in hybrids are (i) do the Nasonia bacterial genomes differ from other animal isolates and (ii) are the hybrid bacterial genomes the same as those in the parental species? Here, we report the cultivation, whole-genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and that, when grown in coculture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent from pathogenic, human associates. Proteus mirabilis from Nasonia vitripennis, Nasonia giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown. IMPORTANCE Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species and host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus, which contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to those in parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.Karissa L. CrossBrittany A. LeighE. Anne HatmakerAram MikaelyanAsia K. MillerSeth R. BordensteinAmerican Society for MicrobiologyarticleProteusProvidenciaNasoniagut bacteriamicrobiomephageMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Proteus Providencia Nasonia gut bacteria microbiome phage Microbiology QR1-502
spellingShingle	Proteus Providencia Nasonia gut bacteria microbiome phage Microbiology QR1-502 Karissa L. Cross Brittany A. Leigh E. Anne Hatmaker Aram Mikaelyan Asia K. Miller Seth R. Bordenstein Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
description	ABSTRACT Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacterium in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterium-assisted lethality in hybrids are (i) do the Nasonia bacterial genomes differ from other animal isolates and (ii) are the hybrid bacterial genomes the same as those in the parental species? Here, we report the cultivation, whole-genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and that, when grown in coculture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent from pathogenic, human associates. Proteus mirabilis from Nasonia vitripennis, Nasonia giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown. IMPORTANCE Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species and host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus, which contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to those in parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.
format	article
author	Karissa L. Cross Brittany A. Leigh E. Anne Hatmaker Aram Mikaelyan Asia K. Miller Seth R. Bordenstein
author_facet	Karissa L. Cross Brittany A. Leigh E. Anne Hatmaker Aram Mikaelyan Asia K. Miller Seth R. Bordenstein
author_sort	Karissa L. Cross
title	Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
title_short	Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
title_full	Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
title_fullStr	Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
title_full_unstemmed	Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
title_sort	genomes of gut bacteria from <italic toggle="yes">nasonia</italic> wasps shed light on phylosymbiosis and microbe-assisted hybrid breakdown
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/7921dd2690744498b5414e2eccba5c47
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Genomes of Gut Bacteria from <italic toggle="yes">Nasonia</italic> Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

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