Bacterial Iron Homeostasis Regulation by sRNAs

Chareyre, Sylvia; Mandin, Pierre

doi:10.1128/microbiolspec.rwr-0010-2017

Cited by 76 publications

(63 citation statements)

References 86 publications

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“…coli . Thus, their repression by RyhB is in line with its role in installing an iron sparing response when iron becomes scarce [17,19]. Before our results, one could have imagined that RyhB represses Nuo and Sdh expression in order to limit accumulation of inactive apo-complexes in iron scarce conditions.…”

Section: Discussionsupporting

confidence: 56%

“…RyhB is one of the most studied sRNAs to date in E . coli [17–19]. RyhB is regulated by Fur, the main regulator of Fe-homeostasis in many bacteria and is expressed during iron starvation [20,21].…”

Section: Introductionmentioning

confidence: 99%

“…RyhB is regulated by Fur, the main regulator of Fe-homeostasis in many bacteria and is expressed during iron starvation [20,21]. When iron becomes limiting in the medium, RyhB base-pairs and represses the translation of more than 100 mRNA targets that encode non-essential iron-utilizing proteins, thus engaging an “iron sparing” response and redirecting iron consumption in the cell [19]. Notably, RyhB was shown to base-pair to the iscRSUA mRNA [16].…”

Section: Introductionmentioning

confidence: 99%

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A small RNA controls bacterial sensitivity to gentamicin during iron starvation

2019

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Phenotypic resistance describes a bacterial population that becomes transiently resistant to an antibiotic without requiring a genetic change. We here investigated the role of the small regulatory RNA (sRNA) RyhB, a key contributor to iron homeostasis, in the phenotypic resistance of Escherichia coli to various classes of antibiotics. We found that RyhB induces phenotypic resistance to gentamicin, an aminoglycoside that targets the ribosome, when iron is scarce. RyhB induced resistance is due to the inhibition of respiratory complexes Nuo and Sdh activities. These complexes, which contain numerous Fe-S clusters, are crucial for generating a proton motive force (pmf) that allows gentamicin uptake. RyhB regulates negatively the expression of nuo and sdh , presumably by binding to their mRNAs and, as a consequence, inhibiting their translation. We further show that Isc Fe-S biogenesis machinery is essential for the maturation of Nuo. As RyhB also limits levels of the Isc machinery, we propose that RyhB may also indirectly impact the maturation of Nuo and Sdh. Notably, our study shows that respiratory complexes activity levels are predictive of the bacterial sensitivity to gentamicin. Altogether, these results unveil a new role for RyhB in the adaptation to antibiotic stress, an unprecedented consequence of its role in iron starvation stress response.

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Section: Discussionsupporting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A small RNA controls bacterial sensitivity to gentamicin during iron starvation

2019

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“…Small regulatory RNAs (sRNAs) act as post-transcriptional regulators controlling bacterial adaptation to environmental changes (Koeppen et al, 2016;Gerrick et al, 2018). Their regulatory functions have become the center of attention in a variety of bacteria, such as E. coli, Salmonella, and Pseudomonas aeruginosa (Koeppen et al, 2016;Chareyre and Mandin, 2018;El Mouali et al, 2018). sRNAs play crucial roles in regulating outer membrane protein expression, iron ion balance, community induction, and bacterial pathogenicity.…”

Section: Introductionmentioning

confidence: 99%

The Transcriptomic and Bioinformatic Characterizations of Iron Acquisition and Heme Utilization in Avibacterium paragallinarum in Response to Iron-Starvation

Huo

Zeng

et al. 2021

Front. Microbiol.

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Avibacterium paragallinarum is the pathogen of infectious coryza, which is a highly contagious respiratory disease of chickens that brings a potentially serious threat to poultry husbandry. Iron is an important nutrient for bacteria and can be obtained from surroundings such as siderophores and hemophores. To date, the mechanisms of iron acquisition and heme utilization as well as detailed regulation in A. paragallinarum have been poorly understood. In this study, we investigated the transcriptomic profiles in detail and the changes of transcriptomes induced by iron restriction in A. paragallinarum using RNA-seq. Compared with the iron-sufficiency control group, many more differentially expressed genes (DEGs) and cellular functions as well as signaling pathways were verified in the iron-restriction group. Among these DEGs, the majority of genes showed decreased expression and some were found to be uniquely present in the iron-restriction group. With an in-depth study of bioinformatic analyses, we demonstrated the crucial roles of the Hut protein and DUF domain-containing proteins, which were preferentially activated in bacteria following iron restriction and contributed to the iron acquisition and heme utilization. Consequently, RT-qPCR results further verified the iron-related DEGs and were consistent with the RNA-seq data. In addition, several novel sRNAs were present in A. paragallinarum and had potential regulatory roles in iron homeostasis, especially in the regulation of Fic protein to ensure stable expression. This is the first report of the molecular mechanism of iron acquisition and heme utilization in A. paragallinarum from the perspective of transcriptomic profiles. The study will contribute to a better understanding of the transcriptomic response of A. paragallinarum to iron starvation and also provide novel insight into the development of new antigens for potential vaccines against infectious coryza by focusing on these iron-related genes.

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“…In E. coli, RyhB is induced upon iron starvation, and it represses the expression of a large set of genes as well as participating in iron homeostasis (Massé and Gottesman, 2002;Chareyre and Mandin, 2018). During iron starvation, it is also involved in sensitivity to colicin Ia, an E. coli-specific bacteriocin produced to kill other E. coli strains (Salvail et al, 2013).…”

Section: Srna-mediated Antimicrobial Responses and Resistancementioning

confidence: 99%

Diversity and Versatility in Small RNA-Mediated Regulation in Bacterial Pathogens

Felden

Augagneur

2021

Front. Microbiol.

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Bacterial gene expression is under the control of a large set of molecules acting at multiple levels. In addition to the transcription factors (TFs) already known to be involved in global regulation of gene expression, small regulatory RNAs (sRNAs) are emerging as major players in gene regulatory networks, where they allow environmental adaptation and fitness. Developments in high-throughput screening have enabled their detection in the entire bacterial kingdom. These sRNAs influence a plethora of biological processes, including but not limited to outer membrane synthesis, metabolism, TF regulation, transcription termination, virulence, and antibiotic resistance and persistence. Almost always noncoding, they regulate target genes at the post-transcriptional level, usually through base-pair interactions with mRNAs, alone or with the help of dedicated chaperones. There is growing evidence that sRNA-mediated mechanisms of actions are far more diverse than initially thought, and that they go beyond the so-called cis- and trans-encoded classifications. These molecules can be derived and processed from 5' untranslated regions (UTRs), coding or non-coding sequences, and even from 3' UTRs. They usually act within the bacterial cytoplasm, but recent studies showed sRNAs in extracellular vesicles, where they influence host cell interactions. In this review, we highlight the various functions of sRNAs in bacterial pathogens, and focus on the increasing examples of widely diverse regulatory mechanisms that might compel us to reconsider what constitute the sRNA.

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Bacterial Iron Homeostasis Regulation by sRNAs

Cited by 76 publications

References 86 publications

A small RNA controls bacterial sensitivity to gentamicin during iron starvation

A small RNA controls bacterial sensitivity to gentamicin during iron starvation

The Transcriptomic and Bioinformatic Characterizations of Iron Acquisition and Heme Utilization in Avibacterium paragallinarum in Response to Iron-Starvation

Diversity and Versatility in Small RNA-Mediated Regulation in Bacterial Pathogens

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