Cargando…

Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)

Arthropods often have obligate relationships with symbiotic microbes, and recent investigations have demonstrated that such host-microbe relationships could be exploited to suppress natural populations of vector carrying mosquitos. Strategies that target the interplay between agricultural pests and...

Descripción completa

Detalles Bibliográficos
Autores principales: Yeoman, Carl J., Brutscher, Laura M., Esen, Özcan C., Ibaoglu, Furkan, Fowler, Curtis, Eren, A. Murat, Wanner, Kevin, Weaver, David K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716498/
https://www.ncbi.nlm.nih.gov/pubmed/31523509
http://dx.doi.org/10.7717/peerj.7548
_version_ 1783447389504274432
author Yeoman, Carl J.
Brutscher, Laura M.
Esen, Özcan C.
Ibaoglu, Furkan
Fowler, Curtis
Eren, A. Murat
Wanner, Kevin
Weaver, David K.
author_facet Yeoman, Carl J.
Brutscher, Laura M.
Esen, Özcan C.
Ibaoglu, Furkan
Fowler, Curtis
Eren, A. Murat
Wanner, Kevin
Weaver, David K.
author_sort Yeoman, Carl J.
collection PubMed
description Arthropods often have obligate relationships with symbiotic microbes, and recent investigations have demonstrated that such host-microbe relationships could be exploited to suppress natural populations of vector carrying mosquitos. Strategies that target the interplay between agricultural pests and their symbionts could decrease the burden caused by agricultural pests; however, the lack of comprehensive genomic insights into naturally occurring microbial symbionts presents a significant bottleneck. Here we employed amplicon surveys, genome-resolved metagenomics, and scanning electron microscopy to investigate symbionts of the wheat stem sawfly (Cephus cinctus), a major pest that causes an estimated $350 million dollars or more in wheat yield losses in the northwestern United States annually. Through 16S rRNA gene sequencing of two major haplotypes and life stages of wheat stem sawfly, we show a novel Spiroplasma species is ever-present and predominant, with phylogenomic analyses placing it as a member of the ixodetis clade of mollicutes. Using state-of-the-art metagenomic assembly and binning strategies we were able to reconstruct a 714 Kb, 72.7%-complete Spiroplasma genome, which represents just the second draft genome from the ixodetis clade of mollicutes. Functional annotation of the Spiroplasma genome indicated carbohydrate-metabolism involved PTS-mediated import of glucose and fructose followed by glycolysis to lactate, acetate, and propionoate. The bacterium also encoded biosynthetic pathways for essential vitamins B2, B3, and B9. We identified putative Spiroplasma virulence genes: cardiolipin and chitinase. These results identify a previously undescribed symbiosis between wheat stem sawfly and a novel Spiroplasma sp., availing insight into their molecular relationship, and may yield new opportunities for microbially-mediated pest control strategies.
format Online
Article
Text
id pubmed-6716498
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher PeerJ Inc.
record_format MEDLINE/PubMed
spelling pubmed-67164982019-09-13 Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus) Yeoman, Carl J. Brutscher, Laura M. Esen, Özcan C. Ibaoglu, Furkan Fowler, Curtis Eren, A. Murat Wanner, Kevin Weaver, David K. PeerJ Agricultural Science Arthropods often have obligate relationships with symbiotic microbes, and recent investigations have demonstrated that such host-microbe relationships could be exploited to suppress natural populations of vector carrying mosquitos. Strategies that target the interplay between agricultural pests and their symbionts could decrease the burden caused by agricultural pests; however, the lack of comprehensive genomic insights into naturally occurring microbial symbionts presents a significant bottleneck. Here we employed amplicon surveys, genome-resolved metagenomics, and scanning electron microscopy to investigate symbionts of the wheat stem sawfly (Cephus cinctus), a major pest that causes an estimated $350 million dollars or more in wheat yield losses in the northwestern United States annually. Through 16S rRNA gene sequencing of two major haplotypes and life stages of wheat stem sawfly, we show a novel Spiroplasma species is ever-present and predominant, with phylogenomic analyses placing it as a member of the ixodetis clade of mollicutes. Using state-of-the-art metagenomic assembly and binning strategies we were able to reconstruct a 714 Kb, 72.7%-complete Spiroplasma genome, which represents just the second draft genome from the ixodetis clade of mollicutes. Functional annotation of the Spiroplasma genome indicated carbohydrate-metabolism involved PTS-mediated import of glucose and fructose followed by glycolysis to lactate, acetate, and propionoate. The bacterium also encoded biosynthetic pathways for essential vitamins B2, B3, and B9. We identified putative Spiroplasma virulence genes: cardiolipin and chitinase. These results identify a previously undescribed symbiosis between wheat stem sawfly and a novel Spiroplasma sp., availing insight into their molecular relationship, and may yield new opportunities for microbially-mediated pest control strategies. PeerJ Inc. 2019-08-27 /pmc/articles/PMC6716498/ /pubmed/31523509 http://dx.doi.org/10.7717/peerj.7548 Text en ©2019 Yeoman et al. https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Agricultural Science
Yeoman, Carl J.
Brutscher, Laura M.
Esen, Özcan C.
Ibaoglu, Furkan
Fowler, Curtis
Eren, A. Murat
Wanner, Kevin
Weaver, David K.
Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
title Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
title_full Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
title_fullStr Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
title_full_unstemmed Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
title_short Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
title_sort genome-resolved insights into a novel spiroplasma symbiont of the wheat stem sawfly (cephus cinctus)
topic Agricultural Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716498/
https://www.ncbi.nlm.nih.gov/pubmed/31523509
http://dx.doi.org/10.7717/peerj.7548
work_keys_str_mv AT yeomancarlj genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT brutscherlauram genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT esenozcanc genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT ibaoglufurkan genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT fowlercurtis genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT erenamurat genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT wannerkevin genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus
AT weaverdavidk genomeresolvedinsightsintoanovelspiroplasmasymbiontofthewheatstemsawflycephuscinctus