Abstract
Summary Streptococcus pyogenes produces a diverse variety of pili in a serotype‐dependent manner and thermosensitive expression of pilus biogenesis genes was previously observed in a serotype M49 strain. However, the precise mechanism and biological significance remain unclear. Herein, the pilus expression analysis revealed the thermosensitive pilus production only in strains possessing the transcriptional regulator Nra. Experimental data obtained for nra deletion and conditional nra‐expressing strains in the background of an M49 strain and the Lactococcus heterologous expression system, indicated that Nra is a positive regulator of pilus genes and also highlighted the importance of the level of intracellular Nra for the thermoregulation of pilus expression. While the nra mRNA level was not significantly influenced by a temperature shift, the Nra protein level was concomitantly increased when the culture temperature was decreased. Intriguingly, a putative stem‐loop structure within the coding region of nra mRNA was a factor related to the post‐transcriptional efficiency of nra mRNA translation. Either deletion of the stem‐loop structure or introduction of silent chromosomal mutations designed to melt the structure attenuated Nra levels, resulting in decreased pilus production. Consequently, the temperature‐dependent translational efficacy of nra mRNA influenced pilus thermoregulation, thereby potentially contributing to the fitness of nra‐positive S. pyogenes in human tissues.
Highlights
Streptococcus pyogenes produces a diverse variety of pili in a serotype-dependent manner and thermosensitive expression of pilus biogenesis genes was previously observed in a serotype M49 strain
Experimental data obtained for nra deletion and conditional nra-expressing strains in the background of an M49 strain and the Lactococcus heterologous expression system, indicated that Nra is a positive regulator of pilus genes and highlighted the importance of the level of intracellular Nra for the thermoregulation of pilus expression
A putative stem-loop structure within the coding region of nra mRNA was a factor related to the post-transcriptional efficiency of nra mRNA translation
Summary
Microorganisms possess intricate mechanisms to expeditiously respond to changes in environmental conditions, such as temperature, pH, salinity, pressure, nutrition and oxygen availability, allowing them to adapt to environmental shifts and avoid deleterious consequences (Bleuven and Landry, 2016; Fang et al, 2016; Papadimitriou et al, 2016; Kraemer and Boynton, 2017). When bacteria are systemically disseminated from the host external surface, their surrounding temperature is significantly increased inside host tissues. Such temperature shifts enable bacteria to frequently modulate transcription, translation and DNA replication efficiency, contributing to pathological processes (de Mendoza, 2014; Guijarro et al, 2015). Two major schemes have been utilized to classify S. pyogenes serotypes. One is based on the antigenicity of the M protein, a major virulence-associated surface protein with a variable region in the N-terminus (Fischetti et al, 1988). Based on the DNA sequence diversity of the 5′ variable region of the emm gene encoding M protein, emm types are currently classified into over 220 types (Beall et al, 1996; Sanderson-Smith et al, 2014).
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