RNase E cleavage shapes the transcriptome of<i>Rhodobacter sphaeroides</i>and strongly impacts phototrophic growth

Förstner, Konrad U.; Reuscher, Carina M.; Haberzettl, Kerstin; Weber, Lennart; Klug, Gabriele

doi:10.26508/lsa.201800080

Cited by 24 publications

(55 citation statements)

References 74 publications

(111 reference statements)

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“…This 5-nt sequence, i.e. ‘RN↓WUU’, is highly similar to previously determined RNase E motifs of Salmonella enterica ( Chao et al, 2017 ) and Rhodobacter sphaeroides ( Förstner et al, 2018 ), indicating that RNase E operates by a conserved mechanism of recognition and cleavage.…”

Section: Resultssupporting

confidence: 77%

Gene autoregulation by 3’ UTR-derived bacterial small RNAs

Hoyos

Huber

Förstner

et al. 2020

eLife

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Negative feedback regulation, that is the ability of a gene to repress its own synthesis, is the most abundant regulatory motif known to biology. Frequently reported for transcriptional regulators, negative feedback control relies on binding of a transcription factor to its own promoter. Here, we report a novel mechanism for gene autoregulation in bacteria relying on small regulatory RNA (sRNA) and the major endoribonuclease, RNase E. TIER-seq analysis (transiently-inactivating-an-endoribonuclease-followed-by-RNA-seq) revealed ~25,000 RNase E-dependent cleavage sites in Vibrio cholerae, several of which resulted in the accumulation of stable sRNAs. Focusing on two examples, OppZ and CarZ, we discovered that these sRNAs are processed from the 3’ untranslated region (3’ UTR) of the oppABCDF and carAB operons, respectively, and base-pair with their own transcripts to inhibit translation. For OppZ, this process also triggers Rho-dependent transcription termination. Our data show that sRNAs from 3’ UTRs serve as autoregulatory elements allowing negative feedback control at the post-transcriptional level.

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Section: Resultssupporting

confidence: 77%

Gene autoregulation by 3’ UTR-derived bacterial small RNAs

Hoyos

Huber

Förstner

et al. 2020

eLife

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“…Thus, the pattern of ompR‐1 induction is in agreement with its RpoHI/RpoHII dependency. Expression patterns for different stresses were also analysed for the sRNA SorX, which is generated from the 3' UTR of the ompR‐1 transcript by the endoribonuclease RNase E (Peng et al ., ; Förstner et al ., ). While increased levels of SorX were observed in response to methylene blue, t‐BOOH, heat and diamide, SDS/EDTA had no significant effect on SorX levels.…”

Section: Discussionmentioning

confidence: 97%

A response regulator of the OmpR family is part of the regulatory network controlling the oxidative stress response of Rhodobacter sphaeroides

Zhao

Peng²,

et al. 2018

Environ Microbiol Rep

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Summary As a free‐living bacterium Rhodobacter sphaeroides needs to respond to many environmental stresses. Oxidative stress, membrane stress or heat stress induce the ompR‐1 gene encoding a protein of the OmpR family. Overexpression of OmpR‐1 results in increased resistance to organic peroxides and diamide. Our data demonstrate that OmpR‐1 positively affects expression of several sRNAs with an established role in R. sphaeroides stress defences and negatively affects the promoter of the rpoHI gene. The RpoHI sigma factor has a main role in the activation of many stress responses. Thus OmpR‐1 has a balancing effect on the activation of the RpoHI regulon. We present a model with OmpR‐1 as part of a regulatory network controlling stress defences in R. sphaeroides.

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“…Many different enzymes, RNA binding proteins and stabilizing or destabilizing RNA elements determine the half-lives of mRNAs [e.g., (Evguenieva-Hackenberg and Klug 2011 )]. In R. sphaeroides reduced RNase E activity strongly impacts phototrophic growth but does not affect doubling time under microaerobic conditions (Förstner et al 2018 ), the reasons for this are not known to date. It was not possible to grow the R. sphaeroides strain with reduced RNase E activity under anaerobic dark conditions so that we could not test the contribution of RNase E to the prolonged iscR and sufB half-lives under these conditions.…”

Section: Discussionmentioning

confidence: 99%

Interplay between formation of photosynthetic complexes and expression of genes for iron–sulfur cluster assembly in Rhodobacter sphaeroides?

et al. 2020

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Formation of photosynthetic complexes leads to a higher demand for Fe–S clusters. We hypothesized that in the facultative phototrophic alpha-proteobacterium Rhodobacter sphaeroides expression of the isc-suf operon for Fe–S cluster formation may be increased under conditions that promote formation of photosynthetic complexes and that, vice versa, lack of the IscR regulator may also affect photosynthesis gene expression. To test this hypothesis, we monitored the activities of the isc-suf sense and anti-sense promoters under different growth conditions and in mutants which are impaired in formation of photosynthetic complexes. We also tested expression of photosynthesis genes in a mutant lacking the IscR regulator. Our results are not in agreement with a co-regulation of the Isc-Suf system and the photosynthetic apparatus at level of transcription. We provide evidence that, coordination of the systems occurs at post-transcriptional levels. Increased levels of isc-suf mRNAs under conditions promoting formation of photosynthetic complexes are due to higher RNA stability.

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RNase E cleavage shapes the transcriptome ofRhodobacter sphaeroidesand strongly impacts phototrophic growth

Abstract: This study identifies the cleavage sites of the endoribonuclease RNase E in the Rhodobacter sphaeroides transcriptome and demonstrates its effect on oxidative stress resistance and phototrophic growth.

Cited by 24 publications

References 74 publications

Gene autoregulation by 3’ UTR-derived bacterial small RNAs

Gene autoregulation by 3’ UTR-derived bacterial small RNAs

A response regulator of the OmpR family is part of the regulatory network controlling the oxidative stress response of Rhodobacter sphaeroides

Interplay between formation of photosynthetic complexes and expression of genes for iron–sulfur cluster assembly in Rhodobacter sphaeroides?

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