Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters.

Dongying Wu, Sean C. Daugherty, Susan E. Van Aken, Grace H. Pai, Kisha L. Watkins, Hoda Khouri, Luke J. Tallon, Jennifer M. Zaborsky, Helen E. Dunbar, Phat L. Tran, Nancy A. Moran, Jonathan A. Eisen

Research output: Contribution to journalArticle

Abstract

Mutualistic intracellular symbiosis between bacteria and insects is a widespread phenomenon that has contributed to the global success of insects. The symbionts, by provisioning nutrients lacking from diets, allow various insects to occupy or dominate ecological niches that might otherwise be unavailable. One such insect is the glassy-winged sharpshooter (Homalodisca coagulata), which feeds on xylem fluid, a diet exceptionally poor in organic nutrients. Phylogenetic studies based on rRNA have shown two types of bacterial symbionts to be coevolving with sharpshooters: the gamma-proteobacterium Baumannia cicadellinicola and the Bacteroidetes species Sulcia muelleri. We report here the sequencing and analysis of the 686,192-base pair genome of B. cicadellinicola and approximately 150 kilobase pairs of the small genome of S. muelleri, both isolated from H. coagulata. Our study, which to our knowledge is the first genomic analysis of an obligate symbiosis involving multiple partners, suggests striking complementarity in the biosynthetic capabilities of the two symbionts: B. cicadellinicola devotes a substantial portion of its genome to the biosynthesis of vitamins and cofactors required by animals and lacks most amino acid biosynthetic pathways, whereas S. muelleri apparently produces most or all of the essential amino acids needed by its host. This finding, along with other results of our genome analysis, suggests the existence of metabolic codependency among the two unrelated endosymbionts and their insect host. This dual symbiosis provides a model case for studying correlated genome evolution and genome reduction involving multiple organisms in an intimate, obligate mutualistic relationship. In addition, our analysis provides insight for the first time into the differences in symbionts between insects (e.g., aphids) that feed on phloem versus those like H. coagulata that feed on xylem. Finally, the genomes of these two symbionts provide potential targets for controlling plant pathogens such as Xylella fastidiosa, a major agroeconomic problem, for which H. coagulata and other sharpshooters serve as vectors of transmission.

Original languageEnglish (US)
JournalPLoS Biology
Volume4
Issue number6
DOIs
StatePublished - Jun 2006
Externally publishedYes

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Fingerprint Dive into the research topics of 'Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters.'. Together they form a unique fingerprint.

  • Cite this

    Wu, D., Daugherty, S. C., Van Aken, S. E., Pai, G. H., Watkins, K. L., Khouri, H., Tallon, L. J., Zaborsky, J. M., Dunbar, H. E., Tran, P. L., Moran, N. A., & Eisen, J. A. (2006). Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biology, 4(6). https://doi.org/10.1371/journal.pbio.0040188