Survival of the drowsiest: the hibernating 100S ribosome in bacterial stress management

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Abstract

In response to nutrient deprivation and environmental insults, bacteria conjoin two copies of non-translating 70S ribosomes that form the translationally inactive 100S dimer. This widespread phenomenon is believed to prevent ribosome turnover and serves as a reservoir that, when conditions become favorable, allows the hibernating ribosomes to be disassembled and recycled for translation. New structural studies have revealed two distinct mechanisms for dimerizing 70S ribosomes, but the molecular basis of the disassembly process is still in its infancy. Many details regarding the sequence of dimerization-dissociation events with respect to the binding and departure of the hibernation factor and its antagonizing disassembly factor remain unclear.

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Reduction of translating ribosomes enables Escherichia coli to maintain elongation rates during slow growth.

Xiongfeng Dai, Manlu Zhu, Mya Warren … (2016)

Bacteria growing under different conditions experience a broad range of demand on the rate of protein synthesis, which profoundly affects cellular resource allocation. During fast growth, protein synthesis has long been known to be modulated by adjusting the ribosome content, with the vast majority of ribosomes engaged at a near-maximal rate of elongation. Here, we systematically characterize protein synthesis by Escherichia coli, focusing on slow-growth conditions. We establish that the translational elongation rate decreases as growth slows, exhibiting a Michaelis-Menten dependence on the abundance of the cellular translational apparatus. However, an appreciable elongation rate is maintained even towards zero growth, including the stationary phase. This maintenance, critical for timely protein synthesis in harsh environments, is accompanied by a drastic reduction in the fraction of active ribosomes. Interestingly, well-known antibiotics such as chloramphenicol also cause a substantial reduction in the pool of active ribosomes, instead of slowing down translational elongation as commonly thought.

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Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population.

Michael J Franklin, Alexander L. Richards, Betsey Pitts … (2012)

Bacteria growing in biofilms are physiologically heterogeneous, due in part to their adaptation to local environmental conditions. Here, we characterized the local transcriptome responses of Pseudomonas aeruginosa growing in biofilms by using a microarray analysis of isolated biofilm subpopulations. The results demonstrated that cells at the top of the biofilms had high mRNA abundances for genes involved in general metabolic functions, while mRNA levels for these housekeeping genes were low in cells at the bottom of the biofilms. Selective green fluorescent protein (GFP) labeling showed that cells at the top of the biofilm were actively dividing. However, the dividing cells had high mRNA levels for genes regulated by the hypoxia-induced regulator Anr. Slow-growing cells deep in the biofilms had little expression of Anr-regulated genes and may have experienced long-term anoxia. Transcripts for ribosomal proteins were associated primarily with the metabolically active cell fraction, while ribosomal RNAs were abundant throughout the biofilms, indicating that ribosomes are stably maintained even in slowly growing cells. Consistent with these results was the identification of mRNAs for ribosome hibernation factors (the rmf and PA4463 genes) at the bottom of the biofilms. The dormant biofilm cells of a P. aeruginosa Δrmf strain had decreased membrane integrity, as shown by propidium iodide staining. Using selective GFP labeling and cell sorting, we show that the dividing cells are more susceptible to killing by tobramycin and ciprofloxacin. The results demonstrate that in thick P. aeruginosa biofilms, cells are physiologically distinct spatially, with cells deep in the biofilm in a viable but antibiotic-tolerant slow-growth state.

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ppGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Gram-positive bacteria.

Rebecca M Corrigan, Lauren E Bellows, Alison Wood-Kaczmar … (2016)

The stringent response is a survival mechanism used by bacteria to deal with stress. It is coordinated by the nucleotides guanosine tetraphosphate and pentaphosphate [(p)ppGpp], which interact with target proteins to promote bacterial survival. Although this response has been well characterized in proteobacteria, very little is known about the effectors of this signaling system in Gram-positive species. Here, we report on the identification of seven target proteins for the stringent response nucleotides in the Gram-positive bacterium Staphylococcus aureus We demonstrate that the GTP synthesis enzymes HprT and Gmk bind with a high affinity, leading to an inhibition of GTP production. In addition, we identified five putative GTPases--RsgA, RbgA, Era, HflX, and ObgE--as (p)ppGpp target proteins. We show that RsgA, RbgA, Era, and HflX are functional GTPases and that their activity is promoted in the presence of ribosomes but strongly inhibited by the stringent response nucleotides. By characterizing the function of RsgA in vivo, we ascertain that this protein is involved in ribosome assembly, with an rsgA deletion strain, or a strain inactivated for GTPase activity, displaying decreased growth, a decrease in the amount of mature 70S ribosomes, and an increased level of tolerance to antimicrobials. We additionally demonstrate that the interaction of ppGpp with cellular GTPases is not unique to the staphylococci, as homologs from Bacillus subtilis and Enterococcus faecalis retain this ability. Taken together, this study reveals ribosome inactivation as a previously unidentified mechanism through which the stringent response functions in Gram-positive bacteria.

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Author and article information

Contributors

Mee-Ngan F. Yap:

ORCID: http://orcid.org/0000-0003-4213-4050

+1 314-977-9241 , meengan.yap@health.slu.edu

Journal

Journal ID (nlm-ta): Curr Genet

Journal ID (iso-abbrev): Curr. Genet

Title: Current Genetics

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 0172-8083

ISSN (Electronic): 1432-0983

Publication date (Electronic): 14 December 2017

Publication date PMC-release: 14 December 2017

Publication date (Print): 2018

Volume: 64

Issue: 4

Pages: 753-760

Affiliations

ISNI 0000 0004 1936 9342, GRID grid.262962.b, Edward A. Doisy Department of Biochemistry and Molecular Biology, , Saint Louis University School of Medicine, ; Saint Louis, MO 63104 USA

Author notes

Communicated by M. Kupiec.

Author information

Mee-Ngan F. Yap http://orcid.org/0000-0003-4213-4050

Article

Publisher ID: 796

DOI: 10.1007/s00294-017-0796-2

PMC ID: 6060826

PubMed ID: 29243175

SO-VID: 502e4414-7e45-4e2e-9449-90f06b05ad98

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 30 November 2017

Date revision received : 9 December 2017

Date accepted : 11 December 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: GM121359

Award Recipient : Mee-Ngan F. Yap

Funded by: Edward Mallinckrodt Jr Foundation

Funded by: The Pew Charitable Trusts

Award ID: 2920

Award Recipient : Mee-Ngan F. Yap

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ScienceOpen disciplines: Genetics

Keywords: ribosome,translation,hpf,hflx,stress response

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ScienceOpen disciplines: Genetics

Keywords: ribosome, translation, hpf, hflx, stress response

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Survival of the drowsiest: the hibernating 100S ribosome in bacterial stress management

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Most cited references 55

Reduction of translating ribosomes enables Escherichia coli to maintain elongation rates during slow growth.

Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population.

ppGpp negatively impacts ribosome assembly affecting growth and antimicrobial tolerance in Gram-positive bacteria.

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Cited by 32

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