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...

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Main Authors: Carl J. Yeoman, Laura M. Brutscher, Özcan C. Esen, Furkan Ibaoglu, Curtis Fowler, A. Murat Eren, Kevin Wanner, David K. Weaver
Format: Article
Language:English
Published: PeerJ Inc. 2019-08-01
Series:PeerJ
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Online Access:https://peerj.com/articles/7548.pdf
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author Carl J. Yeoman
Laura M. Brutscher
Özcan C. Esen
Furkan Ibaoglu
Curtis Fowler
A. Murat Eren
Kevin Wanner
David K. Weaver
author_facet Carl J. Yeoman
Laura M. Brutscher
Özcan C. Esen
Furkan Ibaoglu
Curtis Fowler
A. Murat Eren
Kevin Wanner
David K. Weaver
author_sort Carl J. Yeoman
collection DOAJ
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.
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spelling doaj.art-57a943fe6a0c41908175caf7b46f70022023-12-03T10:54:04ZengPeerJ Inc.PeerJ2167-83592019-08-017e754810.7717/peerj.7548Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)Carl J. Yeoman0Laura M. Brutscher1Özcan C. Esen2Furkan Ibaoglu3Curtis Fowler4A. Murat Eren5Kevin Wanner6David K. Weaver7Department of Animal & Range Sciences, Montana State University, Bozeman, MT, United States of AmericaDepartment of Animal & Range Sciences, Montana State University, Bozeman, MT, United States of AmericaDepartment of Medicine, University of Chicago, Chicago, IL, United States of AmericaDepartment of Animal & Range Sciences, Montana State University, Bozeman, MT, United States of AmericaDepartment of Animal & Range Sciences, Montana State University, Bozeman, MT, United States of AmericaDepartment of Medicine, University of Chicago, Chicago, IL, United States of AmericaDepartment of Plant Sciences & Plant Pathology, Montana State University, Bozeman, MT, United States of AmericaDepartment of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, United States of AmericaArthropods 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.https://peerj.com/articles/7548.pdfSpiroplasmaScanning electron microscopyWheat stem sawflyMetagenomicsMicrobial genomicsPangenomics
spellingShingle Carl J. Yeoman
Laura M. Brutscher
Özcan C. Esen
Furkan Ibaoglu
Curtis Fowler
A. Murat Eren
Kevin Wanner
David K. Weaver
Genome-resolved insights into a novel Spiroplasma symbiont of the Wheat Stem Sawfly (Cephus cinctus)
PeerJ
Spiroplasma
Scanning electron microscopy
Wheat stem sawfly
Metagenomics
Microbial genomics
Pangenomics
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 Spiroplasma
Scanning electron microscopy
Wheat stem sawfly
Metagenomics
Microbial genomics
Pangenomics
url https://peerj.com/articles/7548.pdf
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