The copper-inducible copAB operon in Xanthomonas citri subsp. citri is regulated at transcriptional and translational levels

Freitas, Eliane Cristina de; Ucci, Amanda Piovesan; Teixeira, Elaine Cristina; Pedroso, Gisele Audrei; Hilario, E.; Zocca, Vitória Fernanda Bertolazzi; Paiva, Gabriela Barbosa de; Ferreira, Henrique; Pedrolli, Danielle Biscaro; Bertolini, Maria Célia

doi:10.1099/mic.0.000767

Cited by 8 publications

(6 citation statements)

References 31 publications

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“…However, new paradigms in bacterial gene regulation highlight the role of small regulatory RNAs (sRNAs), acting at a (post-)transcriptional level in disparate stress responses [ 37 , 38 , 39 ]. For instance, sRNAs are involved in a plethora of biological processes, including virulence [ 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 ], antibiotic resistance [ 48 , 49 , 50 , 51 , 52 ] and mobile genetic elements [ 53 ] as well as oxidative and metal stress [ 54 , 55 , 56 , 57 , 58 , 59 , 60 ] and the degradation of organic compounds [ 61 ].…”

Section: Introductionmentioning

confidence: 99%

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

Maertens

Leys

Matroule

2020

Genes

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Bacteria are increasingly used for biotechnological applications such as bioremediation, biorecovery, bioproduction, and biosensing. The development of strains suited for such applications requires a thorough understanding of their behavior, with a key role for their transcriptomic landscape. We present a thorough analysis of the transcriptome of Cupriavidus metallidurans CH34 cells acutely exposed to copper by tagRNA-sequencing. C. metallidurans CH34 is a model organism for metal resistance, and its potential as a biosensor and candidate for metal bioremediation has been demonstrated in multiple studies. Several metabolic pathways were impacted by Cu exposure, and a broad spectrum of metal resistance mechanisms, not limited to copper-specific clusters, was overexpressed. In addition, several gene clusters involved in the oxidative stress response and the cysteine-sulfur metabolism were induced. In total, 7500 transcription start sites (TSSs) were annotated and classified with respect to their location relative to coding sequences (CDSs). Predicted TSSs were used to re-annotate 182 CDSs. The TSSs of 2422 CDSs were detected, and consensus promotor logos were derived. Interestingly, many leaderless messenger RNAs (mRNAs) were found. In addition, many mRNAs were transcribed from multiple alternative TSSs. We observed pervasive intragenic TSSs both in sense and antisense to CDSs. Antisense transcripts were enriched near the 5′ end of mRNAs, indicating a functional role in post-transcriptional regulation. In total, 578 TSSs were detected in intergenic regions, of which 35 were identified as putative small regulatory RNAs. Finally, we provide a detailed analysis of the main copper resistance clusters in CH34, which include many intragenic and antisense transcripts. These results clearly highlight the ubiquity of noncoding transcripts in the CH34 transcriptome, many of which are putatively involved in the regulation of metal resistance.

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Section: Introductionmentioning

confidence: 99%

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

Maertens

Leys

Matroule

2020

Genes

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“…This conservation may suggest a tight homeostatic regulation of Cu across populations of X. fastidiosa. A previous study of homologues of copL in Xanthomonas spp., a gene related with transcriptional and translational regulation of copAB operon, also highlighted the expected conservation of copL in these related pathogens [18]. The sequences for cutC were also highly conserved among the isolates.…”

Section: Phylogenetical Relationships Of Cu-related Genes Copa Copb Copl and Cutc Follows X Fastidiosa Subspecies Classification And Was mentioning

confidence: 65%

Phenotypic and Phylogenetic Characterization of Cu Homeostasis among Xylella fastidiosa Strains

Liu

Cobine

et al. 2021

Pathogens

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Xylella fastidiosa is a bacterial pathogen causing severe diseases and asymptomatic colonization in more than 600 plants worldwide. Copper (Cu) is a widely used antimicrobial treatment for various plant diseases, including those affecting X. fastidiosa hosts. Cu homeostasis among X. fastidiosa strains from different geographical locations and host species has not been characterized. Here, we assessed minimum inhibitory concentration (MIC) of Cu for 54 X. fastidiosa strains. We observed strain-level variation in MIC values within each subspecies. We hypothesized that these differences could be explained by sequence variation in Cu homeostasis genes. Phylogenies based on copA, copB, copL, and cutC were created using 74 genomes (including 43 strains used in vitro) of X. fastidiosa, showing that the phylogenetic clustering of Cu homeostasis associated with clustering was based on core genome phylogenies, rather than on pattern of MIC. No association was found among Cu MIC, subspecies classification, and host and location of isolation, probably due to uneven and limited group of strains whose genomes are available. Further analysis focused on a subgroup of isolates from Georgia’s vineyards that shared similar Cu-related phenotypes. Further research is needed to better understand the distribution of Cu homeostasis for this pathogen.

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“…The extremely low levels of free intracellular copper would prevent low-affinity riboswitches from outcompeting high-affinity copper-binding proteins (Changela et al, 2003), which may be the reason why protein-based post-transcriptional regulation mechanisms have evolved for copper. There are preliminary indications that other families of uORFs post-transcriptionally regulate genes coding for copper export or detoxification systems in response to this metal (de Freitas et al, 2019, Rademacher et al, 2012, Voloudakis et al, 2005). In Rhodobacter capsulatus , the activity of a multi-copper oxidase, CutO, was shown to depend on an upstream ORF with similarities to CruR, CutF, which the authors conjectured works as a Cu chaperone (Öztürk et al, 2021).…”

Section: Resultsmentioning

confidence: 99%

Post-transcriptional regulation by copper with a new upstream Open Reading Frame

Roy

Antoine

Schwartz

et al. 2022

Preprint

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Copper is essential to most living beings but also toxic. Bacteria have thus developed homeostatic mechanisms to tightly control its intracellular concentration. The 3-gene operon bp2923-bfrG-bp2921 is down-regulated by copper and notably encodes a TonB-dependent transporter in Bordetella pertussis. We show that the protein encoded by bp2923, which is a member of the DUF2946 family, represents a new type of upstream Open Reading Frame (uORF) involved in post-transcriptional regulation of the downstream genes. In the absence of copper, the entire operon is transcribed and translated. Perception of copper by the nascent bp2923-coded protein via its conserved CXXC motif triggers Rho-dependent transcription termination between the first and second genes by relieving translation arrest on a conserved C-terminal RAPP motif. Homologues of bp2923 are widespread in bacterial genomes, where they head operons predicted to participate in copper homeostasis. This work has unveiled an original mode of genetic regulation by a transition metal and identified a regulatory function for a member of an uncharacterized family of bacterial proteins that we have named CruR, for copper-responsive upstream regulator.

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The copper-inducible copAB operon in Xanthomonas citri subsp. citri is regulated at transcriptional and translational levels

Cited by 8 publications

References 31 publications

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

The Transcriptomic Landscape of Cupriavidus metallidurans CH34 Acutely Exposed to Copper

Phenotypic and Phylogenetic Characterization of Cu Homeostasis among Xylella fastidiosa Strains

Post-transcriptional regulation by copper with a new upstream Open Reading Frame

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