Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest

ABSTRACT Host-associated microbes display remarkable convergence in genome repertoire resulting from selection to supplement missing host functions. Nutritional supplementation has been proposed in the verrucomicrobial endosymbiont Xiphinematobacter sp., which lives within a globally widespread grou...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Kaitlyn N. Myers, Daniel Conn, Amanda M. V. Brown
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	amino acid biosynthesis comparative genomics genome-wide association study mutualism nutritional symbiont plant-parasitic nematode Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b8a7a616abcf4038b34ae0d959d8edfa
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:b8a7a616abcf4038b34ae0d959d8edfa
record_format	dspace
spelling	oai:doaj.org-article:b8a7a616abcf4038b34ae0d959d8edfa2021-12-02T17:07:26ZEssential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest10.1128/mSystems.01048-202379-5077https://doaj.org/article/b8a7a616abcf4038b34ae0d959d8edfa2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01048-20https://doaj.org/toc/2379-5077ABSTRACT Host-associated microbes display remarkable convergence in genome repertoire resulting from selection to supplement missing host functions. Nutritional supplementation has been proposed in the verrucomicrobial endosymbiont Xiphinematobacter sp., which lives within a globally widespread group of plant-parasitic nematodes that vector damaging nepoviruses to plants. Only one genome sequence has been published from this symbiont, leaving unanswered questions about its diversity, host range, role, and selective pressures within its hosts. Because its hosts are exceptionally resistant to culturing, this symbiont is best studied through advanced genomic approaches. To analyze the role of Xiphinematobacter sp. in its host, sequencing was performed on nematode communities, and then genomes were extracted for comparative genomics, gene ontology enrichment tests, polymorphism analysis, de Bruijn-based genome-wide association studies, and tests of pathway- and site-specific selection on genes predicted play a role in the symbiosis. Results showed a closely clustered set of Xiphinematobacter isolates with reduced genomes of ∼917 kbp, for which a new species was proposed. Symbionts shared only 2.3% of genes with outgroup Verrucomicrobia, but comparative analyses showed high conservation of all 10 essential amino acid (EAA) biosynthesis pathways plus several vitamin pathways. These findings were supported by gene ontology enrichment tests and high polymorphisms in these pathways compared with background. Genome-wide association analysis confirmed high between-species fixation of alleles with significant functional enrichment for EAA and thiamine synthesis. Strong positive selection was detected on sites within these pathways, despite several being under increased purifying selection. Together, these results suggest that supplementation of EAAs missing in the host diet may drive this widespread symbiosis. IMPORTANCE Xiphinematobacter spp. are distinctly evolved intracellular symbionts in the phylum Verrucomicrobia, which includes the important human gut-associated microbe Akkermansia muciniphila and many highly abundant free-living soil microbes. Like Akkermansia sp., Xiphinematobacter sp. is obligately associated with the gut of its hosts, which in this case consists of a group of plant-parasitic nematodes that are among the top 10 most destructive species to global agriculture, by vectoring plant viruses. This study examined the hypothesis that the key to this symbiont’s stable evolutionary association with its host is through provisioning nutrients that its host cannot make that may be lacking in the nematode’s plant phloem diet, such as essential amino acids and several vitamins. The significance of our research is in demonstrating, using population genomics, the signatures of selective pressure on these hypothesized roles to ultimately learn how this independently evolved symbiont functionally mirrors symbionts of phloem-feeding insects.Kaitlyn N. MyersDaniel ConnAmanda M. V. BrownAmerican Society for Microbiologyarticleamino acid biosynthesiscomparative genomicsgenome-wide association studymutualismnutritional symbiontplant-parasitic nematodeMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	amino acid biosynthesis comparative genomics genome-wide association study mutualism nutritional symbiont plant-parasitic nematode Microbiology QR1-502
spellingShingle	amino acid biosynthesis comparative genomics genome-wide association study mutualism nutritional symbiont plant-parasitic nematode Microbiology QR1-502 Kaitlyn N. Myers Daniel Conn Amanda M. V. Brown Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest
description	ABSTRACT Host-associated microbes display remarkable convergence in genome repertoire resulting from selection to supplement missing host functions. Nutritional supplementation has been proposed in the verrucomicrobial endosymbiont Xiphinematobacter sp., which lives within a globally widespread group of plant-parasitic nematodes that vector damaging nepoviruses to plants. Only one genome sequence has been published from this symbiont, leaving unanswered questions about its diversity, host range, role, and selective pressures within its hosts. Because its hosts are exceptionally resistant to culturing, this symbiont is best studied through advanced genomic approaches. To analyze the role of Xiphinematobacter sp. in its host, sequencing was performed on nematode communities, and then genomes were extracted for comparative genomics, gene ontology enrichment tests, polymorphism analysis, de Bruijn-based genome-wide association studies, and tests of pathway- and site-specific selection on genes predicted play a role in the symbiosis. Results showed a closely clustered set of Xiphinematobacter isolates with reduced genomes of ∼917 kbp, for which a new species was proposed. Symbionts shared only 2.3% of genes with outgroup Verrucomicrobia, but comparative analyses showed high conservation of all 10 essential amino acid (EAA) biosynthesis pathways plus several vitamin pathways. These findings were supported by gene ontology enrichment tests and high polymorphisms in these pathways compared with background. Genome-wide association analysis confirmed high between-species fixation of alleles with significant functional enrichment for EAA and thiamine synthesis. Strong positive selection was detected on sites within these pathways, despite several being under increased purifying selection. Together, these results suggest that supplementation of EAAs missing in the host diet may drive this widespread symbiosis. IMPORTANCE Xiphinematobacter spp. are distinctly evolved intracellular symbionts in the phylum Verrucomicrobia, which includes the important human gut-associated microbe Akkermansia muciniphila and many highly abundant free-living soil microbes. Like Akkermansia sp., Xiphinematobacter sp. is obligately associated with the gut of its hosts, which in this case consists of a group of plant-parasitic nematodes that are among the top 10 most destructive species to global agriculture, by vectoring plant viruses. This study examined the hypothesis that the key to this symbiont’s stable evolutionary association with its host is through provisioning nutrients that its host cannot make that may be lacking in the nematode’s plant phloem diet, such as essential amino acids and several vitamins. The significance of our research is in demonstrating, using population genomics, the signatures of selective pressure on these hypothesized roles to ultimately learn how this independently evolved symbiont functionally mirrors symbionts of phloem-feeding insects.
format	article
author	Kaitlyn N. Myers Daniel Conn Amanda M. V. Brown
author_facet	Kaitlyn N. Myers Daniel Conn Amanda M. V. Brown
author_sort	Kaitlyn N. Myers
title	Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest
title_short	Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest
title_full	Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest
title_fullStr	Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest
title_full_unstemmed	Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest
title_sort	essential amino acid enrichment and positive selection highlight endosymbiont's role in a global virus-vectoring pest
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/b8a7a616abcf4038b34ae0d959d8edfa
work_keys_str_mv	AT kaitlynnmyers essentialaminoacidenrichmentandpositiveselectionhighlightendosymbiontsroleinaglobalvirusvectoringpest AT danielconn essentialaminoacidenrichmentandpositiveselectionhighlightendosymbiontsroleinaglobalvirusvectoringpest AT amandamvbrown essentialaminoacidenrichmentandpositiveselectionhighlightendosymbiontsroleinaglobalvirusvectoringpest
_version_	1718381578685513728

Essential Amino Acid Enrichment and Positive Selection Highlight Endosymbiont's Role in a Global Virus-Vectoring Pest

Ejemplares similares