A single synonymous nucleotide change impacts the male-killing phenotype of prophage WO gene wmk

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Abstract

Wolbachia are the most widespread bacterial endosymbionts in animals. Within arthropods, these maternally-transmitted bacteria can selfishly hijack host reproductive processes to increase the relative fitness of their transmitting females. One such form of reproductive parasitism called male killing, or the selective killing of infected males, is recapitulated to degrees by transgenic expression of the WO-mediated killing (wmk) gene. Here, we characterize the genotype-phenotype landscape of wmk-induced male killing in D. melanogaster using transgenic expression. While phylogenetically distant wmk homologs induce no sex-ratio bias, closely-related homologs exhibit complex phenotypes spanning no death, male death, or death of all hosts. We demonstrate that alternative start codons, synonymous codons, and notably a single synonymous nucleotide in wmk can ablate killing. These findings reveal previously unrecognized features of transgenic wmk-induced killing and establish new hypotheses for the impacts of post-transcriptional processes in male killing variation. We conclude that synonymous sequence changes are not necessarily silent in nested endosymbiotic interactions with life-or-death consequences.

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All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 3-6.

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Jessamyn I Perlmutter

Molecular Biosciences, University of Kansas, Lawrence, United States

For correspondence
jessamyn.perlmutter@ku.edu

Competing interests
Jessamyn I Perlmutter, J. Perlmutter and S. Bordenstein are listed as authors on a patent related to the use of wmk in vector control. US Patent 20210000092 16/982708.

"This ORCID iD identifies the author of this article:" 0000-0002-9789-4674
Jane E Meyers

Biological Sciences, Vanderbilt University, Nashville, United States

Competing interests
No competing interests declared.
Seth R Bordenstein

Biological Sciences and Pathology, Microbiology, and Immunology, Vanderbilt University, Nashville, United States

For correspondence
s.bordenstein@vanderbilt.edu

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-7346-0954

Funding

National Institutes of Health (R21 AI133522)

Seth R Bordenstein

National Institutes of Health (F31 AI143152)

Jessamyn I Perlmutter

Vanderbilt Microbiome Initiative (VMI General Funds)

Seth R Bordenstein

National Institutes of Health (P20 GM103418)

Jessamyn I Perlmutter

National Science Foundation (DBI 2109772)

Jessamyn I Perlmutter

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.