Details
| Original language | English |
|---|---|
| Pages (from-to) | 779-795 |
| Number of pages | 17 |
| Journal | Molecular microbiology |
| Volume | 96 |
| Issue number | 4 |
| Publication status | Published - 1 May 2015 |
| Externally published | Yes |
Abstract
Peptidoglycan degradative enzymes have important roles at many stages during the bacterial life cycle, and it is critical that these enzymes be stringently regulated to avoid compromising the integrity of the cell wall. How this regulation is exerted is of considerable interest: promoter-based control and protein-protein interactions are known to be employed; however, other regulatory mechanisms are almost certainly involved. In the actinobacteria, a class of muralytic enzymes - the 'resuscitation-promoting factors' (Rpfs) - orchestrates the resuscitation of dormant cells. In this study, we have taken a holistic approach to exploring the mechanisms governing RpfA function using the model bacterium Streptomyces coelicolor and have uncovered unprecedented multilevel regulation that is coordinated by three second messengers. Our studies show that RpfA is subject to transcriptional control by the cyclic AMP receptor protein, riboswitch-mediated transcription attenuation in response to cyclic di-AMP, and growth stage-dependent proteolysis in response to ppGpp accumulation. Furthermore, our results suggest that these control mechanisms are likely applicable to cell wall lytic enzymes in other bacteria. Streptomyces bacteria have an unusual life cycle, which culminates in the development of dormant spores. Spore germination and outgrowth require the activity of dedicated cell wall-degrading enzymes, the regulation of which is poorly understood. Here, we have uncovered an intricate, multi-level regulatory network orchestrated by three different signaling molecules.
Keywords
- Aconitate Hydratase/genetics, Bacterial Proteins/genetics, Cell Wall/metabolism, Cyclic AMP/metabolism, Cyclic AMP Receptor Protein/genetics, Gene Expression Regulation, Bacterial, Guanine Nucleotides/metabolism, Mutation, Peptidoglycan/metabolism, Promoter Regions, Genetic, Riboswitch/genetics, Second Messenger Systems, Streptomyces coelicolor/enzymology
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology(all)
- Molecular Biology
- Immunology and Microbiology(all)
- Microbiology
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In: Molecular microbiology, Vol. 96, No. 4, 01.05.2015, p. 779-795.
Research output: Contribution to journal › Article › Research › peer review
}
TY - JOUR
T1 - Nucleotide second messenger-mediated regulation of a muralytic enzyme in Streptomyces
AU - St-Onge, Renée J
AU - Haiser, Henry J
AU - Yousef, Mary R
AU - Sherwood, Emma
AU - Tschowri, Natalia
AU - Al-Bassam, Mahmoud
AU - Elliot, Marie A
N1 - Publisher Copyright: © 2015 John Wiley & Sons Ltd. Copyright: Copyright 2015 Elsevier B.V., All rights reserved.
PY - 2015/5/1
Y1 - 2015/5/1
N2 - Peptidoglycan degradative enzymes have important roles at many stages during the bacterial life cycle, and it is critical that these enzymes be stringently regulated to avoid compromising the integrity of the cell wall. How this regulation is exerted is of considerable interest: promoter-based control and protein-protein interactions are known to be employed; however, other regulatory mechanisms are almost certainly involved. In the actinobacteria, a class of muralytic enzymes - the 'resuscitation-promoting factors' (Rpfs) - orchestrates the resuscitation of dormant cells. In this study, we have taken a holistic approach to exploring the mechanisms governing RpfA function using the model bacterium Streptomyces coelicolor and have uncovered unprecedented multilevel regulation that is coordinated by three second messengers. Our studies show that RpfA is subject to transcriptional control by the cyclic AMP receptor protein, riboswitch-mediated transcription attenuation in response to cyclic di-AMP, and growth stage-dependent proteolysis in response to ppGpp accumulation. Furthermore, our results suggest that these control mechanisms are likely applicable to cell wall lytic enzymes in other bacteria. Streptomyces bacteria have an unusual life cycle, which culminates in the development of dormant spores. Spore germination and outgrowth require the activity of dedicated cell wall-degrading enzymes, the regulation of which is poorly understood. Here, we have uncovered an intricate, multi-level regulatory network orchestrated by three different signaling molecules.
AB - Peptidoglycan degradative enzymes have important roles at many stages during the bacterial life cycle, and it is critical that these enzymes be stringently regulated to avoid compromising the integrity of the cell wall. How this regulation is exerted is of considerable interest: promoter-based control and protein-protein interactions are known to be employed; however, other regulatory mechanisms are almost certainly involved. In the actinobacteria, a class of muralytic enzymes - the 'resuscitation-promoting factors' (Rpfs) - orchestrates the resuscitation of dormant cells. In this study, we have taken a holistic approach to exploring the mechanisms governing RpfA function using the model bacterium Streptomyces coelicolor and have uncovered unprecedented multilevel regulation that is coordinated by three second messengers. Our studies show that RpfA is subject to transcriptional control by the cyclic AMP receptor protein, riboswitch-mediated transcription attenuation in response to cyclic di-AMP, and growth stage-dependent proteolysis in response to ppGpp accumulation. Furthermore, our results suggest that these control mechanisms are likely applicable to cell wall lytic enzymes in other bacteria. Streptomyces bacteria have an unusual life cycle, which culminates in the development of dormant spores. Spore germination and outgrowth require the activity of dedicated cell wall-degrading enzymes, the regulation of which is poorly understood. Here, we have uncovered an intricate, multi-level regulatory network orchestrated by three different signaling molecules.
KW - Aconitate Hydratase/genetics
KW - Bacterial Proteins/genetics
KW - Cell Wall/metabolism
KW - Cyclic AMP/metabolism
KW - Cyclic AMP Receptor Protein/genetics
KW - Gene Expression Regulation, Bacterial
KW - Guanine Nucleotides/metabolism
KW - Mutation
KW - Peptidoglycan/metabolism
KW - Promoter Regions, Genetic
KW - Riboswitch/genetics
KW - Second Messenger Systems
KW - Streptomyces coelicolor/enzymology
UR - http://www.scopus.com/inward/record.url?scp=84929207141&partnerID=8YFLogxK
U2 - 10.1111/mmi.12971
DO - 10.1111/mmi.12971
M3 - Article
C2 - 25682701
VL - 96
SP - 779
EP - 795
JO - Molecular microbiology
JF - Molecular microbiology
SN - 0950-382X
IS - 4
ER -