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The ubiquitous aquatic bacteriumCaulobacter crescentus is highly resistant to uranium (U) and facilitates U biomineralization and thus holds promise as an agent of U bioremediation. To gain an understanding of howC. crescentus tolerates U, we employed transposon (Tn) mutagenesis paired with deep sequencing (Tn-seq) in a global screen for genomic elements required for U resistance. Of the 3,879 annotated genes in theC. crescentus genome, 37 were found to be specifically associated with fitness under U stress, 15 of which were subsequently tested through mutational analysis. Systematic deletion analysis revealed that mutants lacking outer membrane transporters (rsaFa andrsaFb ), a stress-responsive transcription factor (cztR ), or a ppGpp synthetase/hydrolase (spoT ) exhibited a significantly lower survival rate under U stress. RsaFa and RsaFb , which are homologues of TolC inEscherichia coli , have previously been shown to mediate S-layer export. Transcriptional analysis revealed upregulation ofrsaFa andrsaFb by 4- and 10-fold, respectively, in the presence of U. We additionally show thatrsaFa mutants accumulated higher levels of U than the wild type, with no significant increase in oxidative stress levels. Our results suggest a function for RsaFa and RsaFb in U efflux and/or maintenance of membrane integrity during U stress. In addition, we present data implicating CztR and SpoT in resistance to U stress. Together, our findings reveal novel gene targets that are key to understanding the molecular mechanisms of U resistance inC. crescentus .IMPORTANCE Caulobacter crescentus is an aerobic bacterium that is highly resistant to uranium (U) and has great potential to be used in U bioremediation, but its mechanisms of U resistance are poorly understood. We conducted a Tn-seq screen to identify genes specifically required for U resistance inC. crescentus . The genes that we identified have previously remained elusive using other omics approaches and thus provide significant insight into the mechanisms of U resistance byC. crescentus . In particular, we show that outer membrane transporters RsaFa and RsaFb , previously known as part of the S-layer export machinery, may confer U resistance by U efflux and/or by maintaining membrane integrity during U stress.

journal of bacteriology

Transposon Mutagenesis Paired with Deep Sequencing of Caulobacter crescentus under Uranium Stress Reveals Genes Essential for Detoxification and Stress Tolerance