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Endosymbiotic Bacteria Are Prevalent and Diverse in Agricultural Spiders

  • Invertebrate Microbiology
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Abstract

Maternally inherited bacterial endosymbionts are common in arthropods, but their distribution and prevalence are poorly characterized in many host taxa. Initial surveys have suggested that vertically transmitted symbionts may be particularly common in spiders (Araneae). Here, we used diagnostic PCR and high-throughput sequencing to evaluate symbiont infection in 267 individual spiders representing 14 species (3 families) of agricultural spiders. We found 27 operational taxonomic units (OTUs) that are likely endosymbiotic, including multiple strains of Wolbachia, Rickettsia, and Cardinium, which are all vertically transmitted and frequently associated with reproductive manipulation of arthropod hosts. Additional strains included Rickettsiella, Spiroplasma, Rhabdochlamydia, and a novel Rickettsiales, all of which could range from pathogenic to mutualistic in their effects upon their hosts. Seventy percent of spider species had individuals that tested positive for one or more endosymbiotic OTUs, and specimens frequently contained multiple symbiotic strain types. The most symbiont-rich species, Idionella rugosa, had eight endosymbiotic OTUs, with as many as five present in the same specimen. Individual specimens within infected spider species had a variety of symbiotypes, differing from one another in the presence or absence of symbiotic strains. Our sample included both starved and unstarved specimens, and dominant bacterial OTUs were consistent per host species, regardless of feeding status. We conclude that spiders contain a remarkably diverse symbiotic microbiota. Spiders would be an informative group for investigating endosymbiont population dynamics in time and space, and unstarved specimens collected for other purposes (e.g., food web studies) could be used, with caution, for such investigations.

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Data Availability

The nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank database under accession numbers MK513512-19, MK521215-57, MK529759-77, MK627518-20, MK631910-40, MK632848-60, MN028387, and the NCBI SRA under PRJNA526944. The datasets analyzed herein are available from the authors upon request.

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Acknowledgments

We thank J. Harwood and J. Dryer for providing and collecting specimens, and three anonymous reviewers for comments on an earlier draft of this manuscript.

Funding

This research work was supported by grants from the Kentucky Science and Engineering Foundation as per Grant/Award Agreements 148-502-10-261 and 148-502-16-377 with the Kentucky Science and Technology Corporation, and the National Institute of Food and Agriculture, U.S. Department of Agriculture (Hatch No. 0224651).

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Authors and Affiliations

  1. Department of Entomology, University of Kentucky, Lexington, KY, 40546, USA

    Jennifer A. White, Alexander Styer, Laura C. Rosenwald, Meghan M. Curry, Kelton D. Welch, Kacie J. Athey & Eric G. Chapman

  2. Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, 94720, USA

    Alexander Styer

  3. Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA, 98801, USA

    Kacie J. Athey

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  1. Jennifer A. White
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Correspondence to Jennifer A. White.

Electronic Supplementary Material

Online Resource 1

Individual spider specimens, diagnostic results, and sequences. Tab1 includes metadata, diagnostic results, COI haplotypes and bacterial strain types associated with each specimen. Tab 2 provides the Genbank accession number and sequences associated with each COI haplotype and bacterial strain type. (XLSX 62 kb)

Online Resource 2

Diagnostic PCR primers. (PDF 120 kb)

Online Resource 3

High throughput read distribution per sample. (XLSX 36 kb)

Online Resource 4

Figs. S1 & S2 Microbiome profile of starved versus unstarved specimens of (Fig. S1) Idionella rugosa and (Fig. S2) Glenognatha foxi. Each profile was generated from a rarified sample of 3000 Illumina MiSeq reads of the V4 region of bacterial 16S rRNA. The 7-8 most common genera are presented in the key for each figure; in Fig. S1, Cardinium, Wolbachia and Rickettsia each encompass two distinct strain type OTUs. In Fig. S2, many of these OTUs could only be placed at the family or order level. (PDF 260 kb)

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White, J.A., Styer, A., Rosenwald, L.C. et al. Endosymbiotic Bacteria Are Prevalent and Diverse in Agricultural Spiders. Microb Ecol 79, 472–481 (2020). https://doi.org/10.1007/s00248-019-01411-w

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