Global discovery of colonization determinants in the squid symbiont vibrio fischeri

John F Brooks Ii, Mattias C. Gyllborg, David C. Cronin, Sarah J. Quillin, Celeste A. Mallama, Ri Foxall, Cheryl Whistler, Andrew L. Goodman, Mark J. Mel*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

70 Scopus citations

Abstract

Animal epithelial tissue becomes reproducibly colonized by specific environmental bacteria. The bacteria (microbiota) perform critical functions for the host's tissue development, immune system development, and nutrition; yet the processes bywhich bacterial diversity in the environment is selected to assemble the correct communities in the host are unclear. To understand the molecular determinants of microbiota selection, we examined colonization of a simplified model in which the light organ of Euprymna scolopes squid is colonized exclusively by Vibrio fischeri bacteria. We applied highthroughput insertion sequencing to identify which bacterial genes are required during host colonization. A library of over 41,000 unique transposon insertions was analyzed before and after colonization of 1,500 squid hatchlings. Mutants that were reproducibly depleted following squid colonization represented 380 genes, including 37 that encode known colonization factors. Validation of select mutants in defined competitions against the wild-type strain identified nine mutants that exhibited a reproducible colonization defect. Some of the colonization factors identified included genes predicted to influence copper regulation and secretion. Other mutants exhibited defects in biofilm development,which is required for aggregation in host mucus and initiation of colonization. Biofilm formation in culture and in vivowas abolished in a strain lacking the cytoplasmic chaperone DnaJ, suggesting an important role for protein quality control during the elaboration of bacterial biofilm in the context of an intact host immune system. Overall these data suggest that cellular stress responses and biofilm regulation are critical processes underlying the reproducible colonization of animal hosts by specific microbial symbionts.

Original languageEnglish (US)
Pages (from-to)17284-17289
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number48
DOIs
StatePublished - Dec 2 2014

Keywords

  • Bacterial colonization |
  • Biofilm |
  • Chaperone |
  • Functional genomics
  • Symbiosis |

ASJC Scopus subject areas

  • General

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