Colocation of Genes Encoding a tRNA-mRNA Hybrid and a Putative Signaling Peptide on Complementary Strands in the Genome of the Hyperthermophilic BacteriumThermotoga maritima

Abstract

In the genome of the hyperthermophilic bacterium Thermotoga maritima, TM0504 encodes a putative signaling peptide implicated in population density-dependent exopolysaccharide formation. Although not noted in the original genome annotation, TM0504 was found to colocate, on the opposite strand, with the gene encoding ssrA, a hybrid of tRNA and mRNA (tmRNA), which is involved in a trans-translation process related to ribosome rescue and is ubiquitous in bacteria. Specific DNA probes were designed and used in real-time PCR assays to follow the separate transcriptional responses of the colocated open reading frames (ORFs) during transition from exponential to stationary phase, chloramphenicol challenge, and syntrophic coculture with Methanococcus jannaschii. TM0504 transcription did not vary under normal growth conditions. Transcription of the tmRNA gene, however, was significantly up-regulated during chloramphenicol challenge and in T. maritima bound in exopolysaccharide aggregates during methanogenic coculture. The significance of the colocation of ORFs encoding a putative signaling peptide and tmRNA in T. maritima is intriguing, since this overlapping arrangement (tmRNA associated with putative small ORFs) was found to be conserved in at least 181 bacterial genomes sequenced to date. Whether peptides related to TM0504 in other bacteria play a role in quorum sensing is not yet known, but their ubiquitous colocalization with respect to tmRNA merits further examination.Although canonical models for bacterial signaling mechanisms have been established (4, 9), chemically diverse molecules that act as mediators for cell-to-cell communication continue to be discovered (42), concomitant with the expanding range of microorganisms found to be involved in inter-and intraspecies communication (18,20,36,42). Recently, signaling has been connected with biologically extreme environments. For example, N-acyl homoserine lactones have been reported in cultures of the haloalkaliphilic archaeon Natronococcus occultus (28). Furthermore, cell density-dependent, peptide-based signaling, tied to formation of exopolysaccharide-based cell aggregates, was identified in the hyperthermophilic bacterium Thermotoga maritima in synthrophic coculture with the hyperthermophilic archaeon Methanococcus jannaschii (10, 11). Presumably, the formation of such aggregates allows M. jannaschii to make methane using the H 2 produced by T. maritima cells as an auto-inhibitory by-product of carbohydrate metabolism (22). During syntrophic coculture of these two organisms, examination of genome-wide transcriptional profiles indicated increased transcript levels of a small hypothetical open reading frame (ORF), annotated as TM0504, in the T. maritima genome (25), in conjunction with up-regulation of adjacent ORFs annotated as putative ABC transporter permease and ATPase subunits (11). Subsequent reexamination of the genomic neighborhood of the TM0504 gene revealed that it was colocated on the complementary strand within the ssrA gene encoding a highly structure...

The genusThermotoga: recent developments

“…Further, analysis of the region around TM0504 revealed that this it was co-located, on the opposite strand with the gene encoding ssrA , a hybrid of tRNA and mRNA (tmRNA), which is involved in a trans- translational process related to ribosome rescue and, is ubiquitous in bacteria [67]. Specific DNA probes were designed and used in real time PCR assays to follow separate transcriptional responses of the co-located ORFs during transition from exponential into stationary phase, chloramphenicol challenge, and syntrophic co-culture with M. jannaschii .…”

Expression of tmRNA in mycobacteria is increased by antimicrobial agents that target the ribosome

“…This suggested that trans ‐translation is important to bacteria for overcoming the effects of ribosome‐targeting antimicrobial agents, although it was not clear whether ribosome inhibition by antimicrobial agents altered the rate of trans ‐translation. Evidence that such agents may affect trans ‐translation came from previous studies reporting that ribosome inhibitors caused an increase in the levels of tmRNA in Thermotoga maritima (Montero et al , 2006) and Streptomyces aureofaciens (Paleckova et al , 2006). However, these studies did not determine whether the changes in tmRNA levels were the result of decreased tmRNA degradation and/or increased synthesis.…”

Bifunctional transfer-messenger RNA

“…tmRNA is abundant in growing cells, but it is further induced by stress conditions such as heat shock, cold shock, and biofilm formation [58-60]. More extensive regulation of tmRNA has been observed in C. crescentus , where the abundances of tmRNA and SmpB change as a function of the cell cycle [61].…”