Genome-resolved insights into a novelSpiroplasmasymbiont of the Wheat Stem Sawfly (Cephus cinctus)

Author:

Yeoman Carl J.1,Brutscher Laura M.12,Esen Özcan C.3,Ibaoglu Furkan12,Fowler Curtis1,Eren A. Murat34,Wanner Kevin5,Weaver David K.6

Affiliation:

1. Department of Animal & Range Sciences, Montana State University, Bozeman, MT, United States of America

2. Department of Microbiology & Immunology, Montana State University, Bozeman, MT, United States of America

3. Department of Medicine, University of Chicago, Chicago, IL, United States of America

4. Marine Biological Laboratory, The Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Woods Hole, Massachuetts, United States of America

5. Department of Plant Sciences & Plant Pathology, Montana State University, Bozeman, MT, United States of America

6. Department of Land Resources and Environmental Sciences, Montana State University, Bozeman, MT, United States of America

Abstract

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 novelSpiroplasmaspecies 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%-completeSpiroplasmagenome, which represents just the second draft genome from the ixodetis clade of mollicutes. Functional annotation of theSpiroplasmagenome 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 putativeSpiroplasmavirulence genes: cardiolipin and chitinase. These results identify a previously undescribed symbiosis between wheat stem sawfly and a novelSpiroplasmasp., availing insight into their molecular relationship, and may yield new opportunities for microbially-mediated pest control strategies.

Funder

Montana Wheat and Barley Committee

Montana Agricultural Experiment Station project

Molecular Biosciences Program (MBSP) and Montana State University

Publisher

PeerJ

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference80 articles.

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2. The defensive Spiroplasma;Ballinger;Current Opinion in Insect Science,2019

3. Effect of wheat stem sawfly damage on yield and quality of selected Canadian spring wheat;Beres;Journal of Economic Entomology,2007

4. Biology and integrated management of wheat stem sawfly and the need for continuing research;Beres;The Canadian Entomologist,2011

5. Arthropod-Spiroplasma relationship in the genomic era;Bolaños;FEMS Microbiology Ecology,2015

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