Translational control plays an important role in the adaptive heat-shock response of Streptomyces coelicolor

Abstract

Stress-induced adaptations require multiple levels of regulation in all organisms to repair cellular damage. In the present study we evaluated the genome-wide transcriptional and translational changes following heat stress exposure in the soil-dwelling model actinomycete bacterium, Streptomyces coelicolor. The combined analysis revealed an unprecedented level of translational control of gene expression, deduced through polysome profiling, in addition to transcriptional changes. Our data show little correlation between the transcriptome and ‘translatome’; while an obvious downward trend in genome wide transcription was observed, polysome associated transcripts following heat-shock showed an opposite upward trend. A handful of key protein players, including the major molecular chaperones and proteases were highly induced at both the transcriptional and translational level following heat-shock, a phenomenon known as ‘potentiation’. Many other transcripts encoding cold-shock proteins, ABC-transporter systems, multiple transcription factors were more highly polysome-associated following heat stress; interestingly, these protein families were not induced at the transcriptional level and therefore were not previously identified as part of the stress response. Thus, stress coping mechanisms at the level of gene expression in this bacterium go well beyond the induction of a relatively small number of molecular chaperones and proteases in order to ensure cellular survival at non-physiological temperatures.

Eliciting the silent lucensomycin biosynthetic pathway in Streptomyces cyanogenus S136 via manipulation of the global regulatory gene adpA

“…These findings demonstrate that transcription of genes for secondary metabolism might be inconsequential to the production of secondary metabolites themselves. Altogether our results caution against overt reliance on transcriptome and translatome data as a proxy to phenotypic expression of actinobacterial BGCs 13,62,63 .…”

Ribosome Profiling of Synechocystis Reveals Altered Ribosome Allocation at Carbon Starvation

“…Several translationally controlled genes reported here can be considered part of a common stress response; an endonuclease, a protease, and thioredoxin M all exhibited increases in protein synthesis without a corresponding increase in mRNA. Translational control of these genes may be a faster way of coordinating their expression than a transcription program (15,22). It is not known whether these genes have a common effector; C i depletion induces many ncRNAs with unknown targets (34).…”

“…For example, antibiotic biosynthesis pathways in Streptomyces coelicolor were found to be "translationally induced" as cells enter stationary phase, as evidenced by increases in translational efficiency for genes in secondary metabolism (14). Also working with Streptomyces coelicolor, Bucca et al reported an increase in translational efficiency of several genes upon temperature shift from 30°C to 42°C (15). Ribosome profiling of Synechocystis during C i depletion might, thus, reveal new mechanisms for how carbon limitation is ultimately transduced to an altered proteome.…”

A cold shock protein promotes high-temperature microbial growth through binding to diverse RNA species

“…Several proteins containing CSD show varied nucleic acid-binding activities that affect gene transcription, DNA replication, and DNA repair, while others interact with mRNA to affect translational efficiency 12 , 13 , 23 , 24 . Recently, the cold shock proteins have been highlighted the likely importance in adaptation to stress that were not previously considered to be part of the heat-shock stimulon in Streptomyces coelicolor 25 . Thus, we hypothesized that proteins containing CSD from thermophilic bacteria, which already show adaptability to high temperatures, might serve as updated stress-response elements to improve high temperature tolerance of other microbes.…”