RNase E and HupB dynamics foster mycobacterial cell homeostasis and fitness

Griego, Anna; Douché, Thibaut; Gianetto, Quentin Giai; Matondo, Mariette; Manina, Giulia

doi:10.1016/j.isci.2022.104233

Cited by 8 publications

(3 citation statements)

References 107 publications

(186 reference statements)

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“…This suggests that BR-bodies help coordinate the multi-step RNA decay process by concentrating essential mRNA decay enzymes with their mRNA substrates, not only to accelerate the rate-limiting step of RNA decay by RNase E, but also to promote the subsequent 3' to 5' exonucleolytic steps that complete mRNA decay, thereby preventing the pre-mature release of RNA decay intermediates. While C. crescentus provides an ideal model for the biochemical characterization of BR-bodies, the RNA degradosome machinery in multiple other bacteria and in mitochondria has been found to form foci in vivo (19,24,(24)(25)(26)(27)(28), and which contain large IDRs, suggesting BR-bodies are likely widespread condensates used for mRNA decay. Biomolecular condensation therefore provides a general organizational strategy for bacteria to organize their biochemical pathways in the absence of membrane-bound organelles.…”

Section: Rnase E Condensates Accelerate 5' Utr Cleavagementioning

confidence: 99%

Caulobacter crescentusRNase E condensation contributes to autoregulation and fitness

Nandana,

Al-Husini,

Vaishnav

et al. 2023

Preprint

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RNase E is the most common RNA decay nuclease in bacteria, setting the global mRNA decay rate and scaffolding formation of the RNA degradosome complex and BR-bodies. To properly set the global mRNA decay rate, RNase E fromEscherichia coliand neighboring γ-proteobacteria were found to autoregulate RNase E levels via the decay of its mRNA’s 5’ UTR. While the 5’ UTR is absent from other groups of bacteria in the Rfam database, we identified that the α-proteobacteriumCaulobacter crescentusRNase E contains a similar 5’ UTR structure that promotes RNase E autoregulation. In both bacteria, the C-terminal IDR of RNase E is required for proper autoregulation to occur, and this IDR is also necessary and sufficient for RNase E to phase-separate, generating BR-bodies. Usingin vitropurified RNase E, we find that the IDR’s ability to promote phase-separation correlates with enhanced 5’ UTR cleavage, suggesting that phase-separation of RNase E with the 5’ UTR enhances autoregulation. Finally, using growth competition experiments we find that a strain capable of autoregulation rapidly outcompetes a strain with a 5’ UTR mutation that cannot autoregulate, suggesting autoregulation promotes optimal cellular fitness.

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Section: Rnase E Condensates Accelerate 5' Utr Cleavagementioning

confidence: 99%

Caulobacter crescentusRNase E condensation contributes to autoregulation and fitness

Nandana,

Al-Husini,

Vaishnav

et al. 2023

Preprint

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“…A typical distribution is the Poisson distribution, with a characteristic an inverse relationship between the coefficient of variation (CV) and the mean copy number (CV 2 = 1/µ). These fluctuations due to the low discrete number of molecules can be supplemented by fluctuations in epigenetic changes, gene regulation, chromosomal neighborhood, RNA synthesis and RNA degradation [89] , [90] , [91] , [92] , [93] , which can increase noise above the Poisson level. Such an increase is prominent when transitions between active and inactive states of a promoter occur rarely and active promoter initiates the transcription of multiple mRNAs in bursts, resulting in a large burst size.…”

Section: Transcriptionmentioning

confidence: 99%

The life and death of RNA across temperatures

Becskei

Rahaman

2022

Computational and Structural Biotechnology Journal

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“…Bacterial ribonucleoprotein bodies (BRbodies) were the first biomolecular condensate discovered in bacteria, composed of the RNA degradosome complex (4). The large intrinsically disordered region (IDR) of RNase E was found to be necessary and sufficient for BR-body formation, and bioinformatic analyses of other bacteria suggest that BR-bodies are likely widespread across phylogeny (2,(4)(5)(6)(7), including for other RNases like RNase Y and J (8,9). Initial characterization of BR-bodies was performed in Caulobacter crescentus, where it was shown that they assemble with poorly translated mRNAs and promote the rapid decay of mRNA (10,11).…”

Section: Introductionmentioning

confidence: 99%

Sinorhizobium melilotiBR-bodies promote fitness during host colonization

Mallikaarachchi,

Huang,

Madras

et al. 2024

Preprint

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Biomolecular condensates, such as the nucleoli or P-bodies, are non-membrane-bound assemblies of proteins and nucleic acids that facilitate specific cellular processes. Like eukaryotic P-bodies, the recently discovered bacterial ribonucleoprotein bodies (BR-bodies) organize the mRNA decay machinery, yet the similarities in molecular and cellular functions across species have been poorly explored. Here, we examine the functions of BR-bodies in the nitrogen-fixing endosymbiont Sinorhizobium meliloti, which colonizes the roots of compatible legume plants. Assembly of BR-bodies into visible foci in S. meliloti cells requires the C-terminal intrinsically disordered region (IDR) of RNase E, and foci fusion is readily observed in vivo, suggesting they are liquid-like condensates that form via mRNA sequestration. Using Rif-seq to measure mRNA lifetimes, we found a global slowdown in mRNA decay in a mutant deficient in BR-bodies, indicating that compartmentalization of the degradation machinery promotes efficient mRNA turnover. While BR-bodies are constitutively present during exponential growth, the abundance of BR-bodies increases upon cell stress, whereby they promote stress resistance. Finally, using Medicago truncatula as host, we show that BR-bodies enhance competitiveness during colonization and appear to be required for effective symbiosis, as mutants without BR-bodies failed to stimulate plant growth. These results suggest that BR-bodies provide a fitness advantage for bacteria during infection, perhaps by enabling better resistance against the host immune response.

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RNase E and HupB dynamics foster mycobacterial cell homeostasis and fitness

Cited by 8 publications

References 107 publications

Caulobacter crescentusRNase E condensation contributes to autoregulation and fitness

Caulobacter crescentusRNase E condensation contributes to autoregulation and fitness

The life and death of RNA across temperatures

Sinorhizobium melilotiBR-bodies promote fitness during host colonization

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