Host-selected mutations converging on a global regulator drive an adaptive leap by bacteria to symbiosis
Abstract
Host immune and physical barriers protect against pathogens but also impede the establishment of essential symbiotic partnerships. To reveal mechanisms by which beneficial organisms adapt to circumvent host defenses, we experimentally evolved ecologically distinct bioluminescent Vibrio fischeri through Euprymna scolopes squid light organs. Serial squid passaging of bacteria produced eight distinct mutations in the binK sensor kinase gene that conferred an exceptional selective advantage demonstrated through both empirical and theoretical analysis. Squid-adaptive binK alleles promoted colonization and immune evasion that was mediated by cell-associated matrices including symbiotic polysaccharide (Syp) and cellulose. binK variation also altered quorum sensing, raising the threshold for luminescence induction. Preexisting coordinate regulation of symbiosis traits by BinK presented an efficient solution where altered BinK function was the key to unlock multiple colonization barriers. These results identify a genetic basis for microbial adaptability and underscore the importance of hosts as selective agents that shape emergent symbiont populations.
Data availability
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Genomes of ancestral and evolved Vibrio fisheriPublicly available at the NCBI BioProject (accession no: PRJNA316342).
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Transcriptomes of ancestral, evolved and mutant binK Vibrio fischeri MJ11Publicly available at the NCBI BioProject (accession no: PRJNA316360).
Article and author information
Author details
Funding
National Science Foundation (IOS-1258099)
- Vaughn S Cooper
- Cheryl A Whistler
U.S. Department of Agriculture (216015)
- Cheryl A Whistler
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Edward G Ruby, University of Hawaii, United States
Version history
- Received: December 19, 2016
- Accepted: April 23, 2017
- Accepted Manuscript published: April 27, 2017 (version 1)
- Version of Record published: June 9, 2017 (version 2)
Copyright
© 2017, Pankey et al.
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.
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