Evolutionary Genetics of Cytoplasmic Incompatibility Genes cifA and cifB in Prophage WO of Wolbachia

Amelia R.I. Lindsey, Danny W. Rice, Sarah R. Bordenstein, Andrew W. Brooks, Seth R. Bordenstein, Irene L.G. Newton

Research output: Contribution to journalArticlepeer-review

91 Scopus citations

Abstract

The bacterial endosymbiont Wolbachia manipulates arthropod reproduction to facilitate its maternal spread through host populations. The most common manipulation is cytoplasmic incompatibility (CI): Wolbachia-infected males produce modified sperm that cause embryonic mortality, unless rescued by embryos harboring the same Wolbachia. The genes underlying CI, cifA and cifB, were recently identified in the eukaryotic association module of Wolbachia's prophage WO. Here, we use transcriptomic and genomic approaches to address three important evolutionary facets of the cif genes. First, we assess whether or not cifA and cifB comprise a classic toxin-antitoxin operon in wMel and show that the two genes exhibit striking, transcriptional differences across host development. They can produce a bicistronic message despite a predicted hairpin termination element in their intergenic region. Second, cifA and cifB strongly coevolve across the diversity of phage WO. Third, we provide new domain and functional predictions across homologs within Wolbachia, and show that amino acid sequences vary substantially across the genus. Finally, we investigate conservation of cifA and cifB and find frequent degradation and loss of the genes in strains that no longer induce CI. Taken together, we demonstrate that cifA and cifB exhibit complex transcriptional regulation in wMel, provide functional annotations that broaden the potential mechanisms of CI induction, and report recurrent erosion of cifA and cifB in non-CI strains, thus expanding our understanding of the most widespread form of reproductive parasitism.

Original languageEnglish (US)
Pages (from-to)434-451
Number of pages18
JournalGenome biology and evolution
Volume10
Issue number2
DOIs
StatePublished - Feb 1 2018
Externally publishedYes

Bibliographical note

Funding Information:
We thank J. Dylan Shropshire, Jeremy Brownlie, and anonymous reviewers for feedback on earlier drafts of the manuscript. This work was supported by the National Science Foundation (DEB 1501227 to A.R.I.L., IOS 1456545 to I.L.G.N., and IOS 1456778 to S.R.B.); the United States Department of Agriculture (NIFA 2016-67011-24778 to A.R.I.L.); the National Institutes of Health (R21 HD086833 and R01 AI132581 to S.R.B.); the Vanderbilt Microbiome Initiative; and Robert and Peggy van den Bosch Memorial Scholarships to A.R.I.L.

Funding Information:
This work was supported by the National Science Foundation (DEB 1501227 to A.R.I.L., IOS 1456545 to I.L.G.N., and IOS 1456778 to S.R.B.); the United States Department of Agriculture (NIFA 2016-67011-24778 to A.R.I.L.); the National Institutes of Health (R21 HD086833 and R01 AI132581 to S.R.B.); the Vanderbilt Microbiome Initiative; and Robert and Peggy van den Bosch Memorial Scholarships to A.R.I.L.

Publisher Copyright:
© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Keywords

  • bacteriophage
  • gene loss
  • prophage
  • reproductive manipulation
  • symbiosis

Fingerprint

Dive into the research topics of 'Evolutionary Genetics of Cytoplasmic Incompatibility Genes cifA and cifB in Prophage WO of Wolbachia'. Together they form a unique fingerprint.

Cite this