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Host infection selects for sRNA variants that drive bacterial social cheating

ABSTRACT: Single-nucleotide mutations in regulatory small RNAs (sRNAs) represent a largely unexplored route to social cheating during bacterial infection. Here we show that arcZ, encoding a conserved Hfq-dependent sRNA in the plant pathogen Dickeya solani, undergoes recurrent single-nucleotide mutations during potato tuber infection. Five distinct arcZ alleles define a graded series of ArcZ functional impairment in which antifungal and protease activities are progressively reduced while virulence is compromised only in a subset of alleles. All five variants gain a fitness advantage exclusively during co-infection with wild-type arcZ1 cells, an advantage that is strongest when variants are rare, declines as cheater frequency increases, and correlates with declining total bacterial productivity, the canonical signature of social cheating and a tragedy of the commons.[kp1.1] No fitness benefit is detected in vitro. Transcriptomic profiling of five arcZ variants identifies a conserved core of 132 downregulated genes enriched in secreted and diffusible functions. Systematic genetic dissection, supported by quantitative proteomics, establishes BudAB-dependent acetoin production as the dominant cooperative public good exploited during co-infection. Wild-type arcZ1 cells divert pyruvate flux toward acetoin via the BudAB pathway, maintaining a less acidic tissue environment that sustains disease progression; arcZ variants, which repress this pathway, exploit the resulting pH buffering without contributing to it. These results establish pleiotropic regulatory sRNAs as a previously unrecognized class of mutational targets for the emergence of social cheaters during host infection.

ORGANISM(S): Dickeya solani

PROVIDER: GSE334754 | GEO | 2026/06/13

REPOSITORIES: GEO

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Project description:The small RNA, ArcZ (previously RyhA/SraH), was discovered in several genome-wide screens in Escherichia coli and Salmonella. Its high degree of genomic conservation, its frequent recovery by shotgun sequencing, and its association with the RNA chaperone, Hfq, identified ArcZ as an abundant enterobacterial âcoreâ small RNA of unknown function. Here, we report that ArcZ acts as a post-transcriptional regulator in Salmonella, repressing the mRNAs of the widely distributed sdaCB (serine uptake) and tpx (oxidative stress) genes, and of STM3216, a horizontally acquired methyl-accepting chemotaxis protein (MCP). Both sdaCB and STM3216 are regulated by sequestration of the ribosome binding site. In contrast, the tpx mRNA is targeted in the coding sequence (CDS), arguing that CDS targeting is more common than appreciated. Transcriptomic analysis of an arcZ deletion strain further argued for the existence of a distinct set of Salmonella loci specifically regulated by ArcZ. In contrast, increased expression of the sRNA altered the steady-state levels of >16% (â¥750) of all Salmonella mRNAs, and rendered the bacteria non-motile. Deep sequencing detected a dramatically changed profile of Hfq-bound sRNAs and mRNAs suggesting that the unprecedented degree of pleiotropic regulation might in part be caused by titration of Hfq binding by ArcZ. This study used three different approaches to identify target genes and biological role of the small RNA ArcZ in Salmonella Typhimurium. Transcriptomic analysis of ArcZ overexpression: Strain JVS-0082 (ÎarcZ) was transformed with plasmids pJV300 (control) and pKP48-1 (parcZ), and grown in liquid culture (LB broth) inoculated 1:100 from an overnight culture for 6h after cells had reached an OD600=2.0 to attain late stationary phase. Transcriptomic analysis of arcZ mutant strain: Strains JVS-007 (WT) and JVS-0082 (ÎarcZ) were transformed with plasmid pJV300 (control) and grown in liquid culture (LB broth) inoculated 1:100 from an overnight culture for 6h after cells had reached an OD600=2.0 to attain late stationary phase. Transcriptional effects of ArcZ pulse expression: Strain SL1344 was transformed with plasmids pKP8-35 (pBAD-control) and pKP4-13 (pBAD-ArcZ), and grown in liquid culture (LB broth) inoculated 1:100 from an overnight culture to an OD600 of 1.5. Expression of the insert was induced with L-arabinose (0.2% final concentrations) for 10 min. Three biological replicates were performed for each strain/condition.

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Host infection selects for sRNA variants that drive bacterial social cheating

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