Abstract
Control of mRNA translation is a crucial regulatory mechanism used by bacteria to respond to their environment. In the soil bacterium Pseudomonas fluorescens, RimK modifies the C-terminus of ribosomal protein RpsF to influence important aspects of rhizosphere colonisation through proteome remodelling. In this study, we show that RimK activity is itself under complex, multifactorial control by the co-transcribed phosphodiesterase trigger enzyme (RimA) and a polyglutamate-specific protease (RimB). Furthermore, biochemical experimentation and mathematical modelling reveal a role for the nucleotide second messenger cyclic-di-GMP in coordinating these activities. Active ribosome regulation by RimK occurs by two main routes: indirectly, through changes in the abundance of the global translational regulator Hfq and directly, with translation of surface attachment factors, amino acid transporters and key secreted molecules linked specifically to RpsF modification. Our findings show that post-translational ribosomal modification functions as a rapid-response mechanism that tunes global gene translation in response to environmental signals.
Highlights
The plant rhizosphere is a highly complex environment, comprising an intricate spatial organisation of roots and soil, with thousands of competing and cooperating microorganisms linked by dynamic fluxes of nutrients, toxins and signalling molecules [1, 2]
In the soil bacterium Pseudomonas fluorescens, root colonisation is controlled by RimK, a glutamate ligase found in many different bacterial species
We examine the consequences of this ribosomal modification for mRNA translation and bacterial behaviour
Summary
The plant rhizosphere is a highly complex environment, comprising an intricate spatial organisation of roots and soil, with thousands of competing and cooperating microorganisms linked by dynamic fluxes of nutrients, toxins and signalling molecules [1, 2]. Microbial rhizosphere colonisation is a correspondingly complex, multi-stage process by which soil-associated bacteria spatially explore, exploit and defend the root environment [3]. To enable effective rhizosphere colonisation, soil bacteria sense many different environmental inputs and translate them into an integrated phenotypic response. This requires an interconnected network of signal transduction systems functioning at multiple regulatory levels, including gene transcription [6], modulation of translational activity [7] and changes in protein function [8]. CdG signalling in Pseudomonas forms a highly complex, non-linear and pleiotropic network, with multiple connections to other signalling systems and phenotypic outputs that vary profoundly in response to environmental cues [14, 15]. Pseudomonas cdG signalling shows extensive overlap with other global gene regulators, such as Gac/Rsm [17, 18] and the RNA-chaperone Hfq [19]
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