Role of a cryptic tRNA gene operon in survival under translational stress

Abstract

As compared to eukaryotes, bacteria have a reduced tRNA gene set encoding between 30 and 220 tRNAs. Although in most bacterial phyla tRNA genes are dispersed in the genome, many species from distinct phyla also show genes forming arrays. Here, we show that two types of arrays with distinct evolutionary origins exist. This work focuses on long tRNA gene arrays (L-arrays) that encompass up to 43 genes, which disseminate by horizontal gene transfer and contribute supernumerary tRNA genes to the host. Although in the few cases previously studied these arrays were reported to be poorly transcribed, here we show that the L-array of the model cyanobacterium Anabaena sp. PCC 7120, encoding 23 functional tRNAs, is largely induced upon impairment of the translation machinery. The cellular response to this challenge involves a global reprogramming of the transcriptome in two phases. tRNAs encoded in the array are induced in the second phase of the response, directly contributing to cell survival. Results presented here show that in some bacteria the tRNA gene set may be partitioned between a housekeeping subset, which constantly sustains translation, and an inducible subset that is generally silent but can provide functionality under particular conditions.

Distribution and genomic variation of thermophilic cyanobacteria in diverse microbial mats at the upper temperature limits of photosynthesis

“…Two gene clusters enriched in the A’-like clade of the A/B-lineage pangenome are those encoding a tRNA-splicing ligase, RtcB, a predicted archease involved in RtcB activation, and a tRNA methyltransferase, trmH (Supplementary File 3). Archaease and RtcB are conserved across all domains of life (Desai et al, 2014) and are thought to assist in recovery from stress-induced tRNA damage (Santamaría-Gómez et al, 2021; Tanaka & Shuman, 2011), while TrmH is implicated in regulating transcriptional response to stress conditions in E. coli (Galvanin et al, 2020). Archease sequences were only recovered from A’-like MAGs and the OS-A genome.…”

CvkR is a MerR-type transcriptional repressor of class 2 type V-K CRISPR-associated transposase systems

“…Differentially expressed genes outside the AnCAST system included the L-array, a cryptic tRNA gene cluster relevant for survival under translational stress 36 , which was upregulated here in Δ cvkR Com (Fig. 4g ), inverse to the regulation observed for cas12k and tnsB .…”

Distribution and Genomic Variation of Thermophilic Cyanobacteria in Diverse Microbial Mats at the Upper Temperature Limits of Photosynthesis

“…Two gene clusters enriched in the A′-like clade of the A/B-lineage pangenome are those encoding a tRNA-splicing ligase, RtcB, a predicted archease involved in RtcB activation, and a tRNA methyltransferase, TrmH ( Data Set S3 ). Archease and RtcB are conserved across all domains of life ( 61 ) and are thought to assist in recovery from stress-induced tRNA damage ( 62 , 63 ), while TrmH is implicated in regulating transcriptional response to stress conditions in Escherichia coli ( 64 ). Archease sequences were recovered only from A′-like MAGs and the OS-A genome.…”