Control of mRNA translation by dynamic ribosome modification

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 Cterminus 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.

Plasmid manipulation of bacterial behaviour through translational regulatory crosstalk

“…Hfq controls multiple phenotypes in SBW25 (7), however the effects of Hfq dysregulation upon rsmQ deletion appeared to be modest, particularly when compared to secondary Hfq control by the RimABK system, for example (7,78). An intriguing possibility is that the plasmid-borne Hfq homologue pQBR0137, whose abundance increases in the absence of rsmQ, may compensate for reduced chromosomal Hfq activity.…”

“…The presence of multiple, interconnected layers of regulation make signalling phenotypes challenging to interrogate in a laboratory setting. For example, Hfq is global master regulator of translation (7,55) and has an overlapping regulon with the Rsm proteins (76) as well as circumstances in which Hfq and RsmA directly interact (77), adding further regulatory complexity.…”

“…Although transcriptional regulation is important for bacterial survival and adaptation, bacteria also rely on translational regulation to respond to changes in their environment (5). Bacteria are able to exert this control by deploying second messenger signals (6), directly altering the ribosome (7) or impacting mRNA stability and accessibility via pathways such as Gac-Rsm (8, 9). It is currently unknown whether conjugative plasmids are able to manipulate translational regulatory pathways.…”

The Multiple Regulatory Relationship Between RNA-Chaperone Hfq and the Second Messenger c-di-GMP

“…RimK is, intriguingly, an ATP-dependent glutamate ligase (Kang et al, 1989) that can append glutamate residues to the C-terminus of protein S6 (RpsF) located in the ribosomal 30S subunit (Zhao G. et al, 2013). By regulating the function of the posttranslational modification of ribosomal protein RpsF, RimK can control the translation of some relevant proteins (Kino et al, 2011;Grenga et al, 2020). Studies have shown that RimA, RimB and c-di-GMP can all activate RimK (Figure 4C).…”

Going virtual: a report from the sixth Young Microbiologists Symposium on ‘Microbe Signalling, Organisation and Pathogenesis’

“…RimB ensures that glutamate chains on RpsF are formed in units of four. All three proteins interact, and their function maintains a fine balance of translational control in response to low temperature, nutrient deprivation and c-di-GMP concentration, which are known to regulate expression of the operon [15].…”