Characterization of the BolA Homolog IbaG: A New Gene Involved in Acid Resistance

Guinote, Inês Batista; Moreira, Ricardo Neves; Freire, Patrick; Arraiano, Cecília M.

doi:10.4014/jmb.1107.07037

Cited by 19 publications

(32 citation statements)

References 28 publications

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“…YrbA is an homologous protein of BolA and was very recently renamed IbaG ( i nduced b y a cid g ene) in E . coli [92]. IbaG doesn’t share the morphogene properties of BolA and its enzymatic activity was not analysed but it seems to act as a transcriptional regulator to protect the cell against stress.…”

Section: Resultsmentioning

confidence: 99%

Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera

2013

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BackgroundBuchnera aphidicola is an obligate symbiotic bacterium, associated with most of the aphididae, whose genome has drastically shrunk during intracellular evolution. Gene regulation in Buchnera has been a matter of controversy in recent years as the combination of genomic information with the experimental results has been contradictory, refuting or arguing in favour of a functional and responsive transcription regulation in Buchnera.The goal of this study was to describe the gene transcription regulation capabilities of Buchnera based on the inventory of cis- and trans-regulators encoded in the genomes of five strains from different aphids (Acyrthosiphon pisum, Schizaphis graminum, Baizongia pistacea, Cinara cedri and Cinara tujafilina), as well as on the characterisation of some intrinsic structural properties of the DNA molecule in these bacteria.ResultsInteraction graph analysis shows that gene neighbourhoods are conserved between E. coli and Buchnera in structures called transcriptons, interactons and metabolons, indicating that selective pressures have acted on the evolution of transcriptional, protein-protein interaction and metabolic networks in Buchnera. The transcriptional regulatory network in Buchnera is composed of a few general DNA-topological regulators (Nucleoid Associated Proteins and topoisomerases), with the quasi-absence of any specific ones (except for multifunctional enzymes with a known gene expression regulatory role in Escherichia coli, such as AlaS, PepA and BolA, and the uncharacterized hypothetical regulators YchA and YrbA). The relative positioning of regulatory genes along the chromosome of Buchnera seems to have conserved its ancestral state, despite the genome erosion. Sigma-70 promoters with canonical thermodynamic sequence profiles were detected upstream of about 94% of the CDS of Buchnera in the different aphids. Based on Stress-Induced Duplex Destabilization (SIDD) measurements, unstable σ70 promoters were found specifically associated with the regulator and transporter genes.ConclusionsThis genomic analysis provides supporting evidence of a selection of functional regulatory structures and it has enabled us to propose hypotheses concerning possible links between these regulatory elements and the DNA-topology (i.e., supercoiling, curvature, flexibility and base-pair stability) in the regulation of gene expression in the shrunken genome of Buchnera.

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Section: Resultsmentioning

confidence: 99%

Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera

2013

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“…56 These acid conditions would presumably impact the Grx4-IbaG Fe-S coordination environment, possibly altering the lability or binding affinity of the Fe-S cluster. Interestingly, previous genetic studies have implicated ibaG in resistance against acid stress, 35 which might involve the pH-sensitive [2Fe-2S]-bridged Grx4-IbaG heterodimer.…”

Section: Discussionmentioning

confidence: 99%

“…Consequently, yrbA was renamed ibaG ( i nfluenced b y a cid g ene). 35 Similar to BolA, IbaG may have a function in cell wall biosynthesis, as genes found in the vicinity of ibaG are involved in maintenance of the outer membrane and cell wall. In addition, similar to grxD, ibaG displays an aggravating interaction with isc pathway components in a genome-wide synthetic lethality/sickness screen, suggesting that IbaG may function with the Suf proteins in Fe-S cluster assembly or sulfur donation.…”

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confidence: 99%

The Escherichia coli BolA Protein IbaG Forms a Histidine-Ligated [2Fe-2S]-Bridged Complex with Grx4

Dlouhy

Albetel

et al. 2016

Biochemistry

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Two ubiquitous protein families have emerged as key players in iron metabolism, the CGFS type monothiol glutaredoxins (Grxs) and the BolA proteins. Monothiol Grxs and BolA proteins form heterocomplexes that have been implicated in Fe-S cluster assembly and trafficking. The E. coli genome encodes members of both of these proteins families, namely the monothiol glutaredoxin Grx4, and two BolA family proteins, BolA and IbaG. Previous work has demonstrated that E. coli Grx4 and BolA interact as both apo and [2Fe-2S]-bridged heterodimers that are spectroscopically distinct from [2Fe-2S]-bridged Grx4 homodimers. However, the physical and functional interactions between Grx4 and IbaG are uncharacterized. Here we show that co-expression of Grx4 with IbaG yields a [2Fe-2S]-bridged Grx4-IbaG heterodimer. In vitro interaction studies indicate that IbaG binds the [2Fe-2S] Grx4 homodimer to form apo Grx4-IbaG heterodimers as well as the [2Fe-2S] Grx4-IbaG heterodimer, altering the cluster stability and coordination environment. Additionally, spectroscopic and mutagenesis studies provide evidence that IbaG ligates the Fe-S cluster via the conserved histidine that is present in all BolA proteins and by a second conserved histidine that is present in the H/C loop of two of the four classes of BolA proteins. These results suggest that IbaG may function in Fe-S cluster assembly and trafficking in E. coli as demonstrated for other BolA homologues that interact with monothiol Grxs.

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“…E. coli , like many other organisms, encodes more than one BolA family protein. In addition to the 105 amino acid protein BolA , E. coli encodes IbaG (formerly YrbA), an 84 amino acid protein that also contains the characteristic class II KH fold of BolA proteins (14). Unlike BolA, neither overexpression nor the absence of IbaG alters E. coli cell shape; however, overexpression of ibaG is deleterious to bacterial growth, while its deletion enhanced bacterial growth (14).…”

Section: Introductionmentioning

confidence: 99%

“…In addition to the 105 amino acid protein BolA , E. coli encodes IbaG (formerly YrbA), an 84 amino acid protein that also contains the characteristic class II KH fold of BolA proteins (14). Unlike BolA, neither overexpression nor the absence of IbaG alters E. coli cell shape; however, overexpression of ibaG is deleterious to bacterial growth, while its deletion enhanced bacterial growth (14). IbaG expression is induced in response to acid, accounting for its name, I nfluenced b y a cid g ene, and the absence of ibaG also increases E. coli sensitivity to acid stress.…”

Section: Introductionmentioning

confidence: 99%

AVibrio choleraeBolA-like protein is required for proper cell shape and cell envelope integrity

Fleurie

Zoued

Álvarez

et al. 2019

Preprint

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25BolA family proteins are conserved in gram-negative bacteria and many eukaryotes. 26 While diverse cellular phenotypes have been linked to this protein family, the molecular 27 pathways through which these proteins mediate their effects are not well-described. Here, 28 we investigated the role of BolA family proteins in Vibrio cholerae, the cholera pathogen. 29 Like Escherichia coli, V. cholerae encodes two BolA proteins, BolA and IbaG. However, 30 in marked contrast to E. coli, where bolA is linked to cell shape and ibaG is not, in V. 31 cholerae, bolA mutants lack morphological defects, whereas ibaG proved critical for the 32 generation and/or maintenance of the pathogen's morphology. Notably, the bizarre-33 shaped, multi-polar, elongated and wide cells that predominated in exponential phase 34 ΔibaG V. cholerae cultures were not observed in stationary phase cultures. The V. 35 cholerae ΔibaG mutant exhibited increased sensitivity to cell envelope stressors, 36 including cell wall acting antibiotics and bile, and was defective in intestinal colonization. 37 ΔibaG V. cholerae had reduced peptidoglycan and lipid II and altered outer membrane 38 lipids, likely contributing to the mutant's morphological defects and sensitivity to envelope 39 stressors. Transposon-insertion sequencing analysis of ibaG's genetic interactions 40 suggested that ibaG is involved in several processes involved in the generation and 41 homeostasis of the cell envelope. Furthermore, co-purification studies revealed that IbaG 42 interacts with proteins containing iron-sulfur clusters or involved in their assembly. 43 Collectively, our findings suggest that V. cholerae IbaG controls cell morphology and cell 44 envelope integrity through its role in biogenesis or trafficking of iron-sulfur cluster proteins. 45 46 47 3 Importance 48BolA-like proteins are conserved across prokaryotes and eukaryotes. These proteins 49 have been linked to a variety of phenotypes, but the pathways and mechanisms through 50 which they act have not been extensively characterized. Here, we unraveled the role of 51 the BolA-like protein IbaG in the cholera pathogen Vibrio cholerae. The absence of IbaG 52 was associated with dramatic changes in cell morphology, sensitivity to envelope 53 stressors, and intestinal colonization defects. IbaG was found to be required for 54 biogenesis of several components of the V. cholerae cell envelope and to interact with 55 numerous iron-sulfur cluster containing proteins and factors involved in their assembly. 56 Thus, our findings suggest that IbaG governs V. cholerae cell shape and cell envelope 57 homeostasis through its effects on iron-sulfur proteins and associated pathways. The 58 diversity of processes involving iron-sulfur containing proteins is likely a factor underlying 59 the range of phenotypes associated with BolA family proteins. 60 61 4 62The BolA protein family is widely conserved across gram-negative bacteria and 63 eukaryotes (1). These proteins have been linked to a range ...

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Characterization of the BolA Homolog IbaG: A New Gene Involved in Acid Resistance

Cited by 19 publications

References 28 publications

Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera

Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera

The Escherichia coli BolA Protein IbaG Forms a Histidine-Ligated [2Fe-2S]-Bridged Complex with Grx4

AVibrio choleraeBolA-like protein is required for proper cell shape and cell envelope integrity

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