The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability

Todd, Jonathan D.; Sawers, R. Gary; Rodionov, Dmitry A.; Johnston, Andrew

doi:10.1007/s00438-006-0115-y

Cited by 48 publications

(84 citation statements)

References 58 publications

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“…The ability of the Irr from A. tumefaciens to positively and negatively regulate target genes is similar to that observed in B. japonicum (44,56). As was observed in R. leguminosarum, Irr also inhibits the transcription of rirA, the other iron-responsive regulator in A. tumefaciens (64). RirA inhibits iron uptake systems, as shown here and in previous work by Ngok-Ngam et al (43).…”

Section: Discussionsupporting

confidence: 88%

“…In contrast, the expression of the Fe-S cluster synthesis operon (nifS) appears to be inhibited by RirA under high-iron conditions. RirA is thought to respond to iron indirectly via association with Fe-S clusters and is a member of the Rrf2 family of transcription regulators, which also includes the E. coli regulator IscR (64). Members of this family often contain three conserved cysteine residues, which in the case of RirA from A. tumefaciens are located at residues 91, 99, and 105 (55).…”

Section: Discussionmentioning

confidence: 99%

“…The expression of a large number of genes is altered in an R. leguminosarum rirA mutant (63). Although direct binding of RirA to DNA has not been reported, a DNA sequence necessary for RirA-dependent regulation was identified (63,64,75). The ligand that imparts iron responsiveness to RirA has not been established, although the related Rrf2-type protein IscR binds and responds to Fe-S clusters, and it has been suggested that RirA also binds Fe-S clusters (19,31,58).…”

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confidence: 99%

“…The role of Irr and its potential interplay with RirA, however, remain unstudied. In R. leguminosarum, transcriptional studies have shown that Irr and RirA coregulate a wide range of iron-associated genes, including rirA (64). It is likely that the iron response circuitry in A. tumefaciens is similarly intertwined, and understanding this circuitry requires examination of both regulators in parallel.…”

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confidence: 99%

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Antiparallel and Interlinked Control of Cellular Iron Levels by the Irr and RirA Regulators of Agrobacterium tumefaciens

Hibbing

Fuqua

2011

J Bacteriol

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The plant pathogen Agrobacterium tumefaciens encodes predicted iron-responsive regulators, Irr and RirA, that function in several other bacteria to control the response to environmental iron levels. Deletion mutations of irr and rirA, alone and in combination, were evaluated for their impact on cellular iron response. Growth was severely diminished in the ⌬irr mutant under iron-limiting conditions, but reversed to wild-type levels in an ⌬irr ⌬rirA mutant. The level of uncomplexed iron in the ⌬irr mutant was decreased, whereas the ⌬rirA mutant exhibited elevated iron levels. Sensitivity of the ⌬irr and ⌬rirA mutants to iron-activated antimicrobial compounds generally reflected their uncomplexed-iron levels. Expression of genes that encode iron uptake systems was decreased in the ⌬irr mutant, whereas that of iron utilization genes was increased. Irr function required a trihistidine repeat likely to mediate interactions with heme. Iron uptake genes were derepressed in the ⌬rirA mutant. In the ⌬irr ⌬rirA mutant, iron uptake and utilization genes were derepressed, roughly combining the phenotypes of the single mutants. Siderophore production was elevated in the rirA mutant, but most strongly regulated by an RirA-controlled sigma factor. Expression of rirA itself was regulated by Irr, RirA, and iron availability, in contrast to irr expression, which was relatively stable in the different mutants. These studies suggest that in A. tumefaciens, the Irr protein is most active under low-iron conditions, inhibiting iron utilization and activating iron acquisition, while the RirA protein is active under high-iron conditions, repressing iron uptake.

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Section: Discussionsupporting

confidence: 88%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Antiparallel and Interlinked Control of Cellular Iron Levels by the Irr and RirA Regulators of Agrobacterium tumefaciens

Hibbing

Fuqua

2011

J Bacteriol

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“…4), which is consistent with the notion that Irr and RirA are sufS2 repressors under low iron and high iron conditions, respectively (Hibbing & Fuqua, 2011;Todd et al, 2006). The derepression of sufS2-lacZ in the irr and rirA mutant strains (WK074/pBBR and PN094/pBBR) was fully reversed in the complemented strains WK074/pIRR and PN094/pRIRA (Fig.…”

Section: The Sufs2 Gene Is Required For Rira Activitysupporting

confidence: 88%

Cysteine desulphurase-encoding gene sufS2 is required for the repressor function of RirA and oxidative resistance in Agrobacterium tumefaciens

et al. 2014

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The Agrobacterium tumefaciens genome contains a cluster of genes that are predicted to encode Fe-S cluster assembly proteins, and this cluster is known as the sufS2BCDS1XA operon. sufS2 is the first gene in the operon, and it was inactivated to determine its physiological function. The sufS2 mutant exhibited a small colony phenotype, grew slower than the wild-type strain and was more sensitive to various oxidants including peroxide, organic hydroperoxide and superoxide. The sufS2 gene was negatively regulated by iron response regulator (Irr) and rhizobial iron regulator (RirA) under low and high iron conditions, respectively, and was inducible in response to oxidative stress. The oxidant-induced expression of sufS2 was controlled by Irr, RirA and an additional but not yet identified mechanism. sufS2 was required for RirA activity in the repression of a sufS2 promoter-lacZ fusion. RirA may use Fe-S as its cofactor. sufS2 disruption may cause a defect in the Fe-S supply and could thereby affect the RirA activity. The three conserved cysteine residues (C91, C99 and C105) in RirA were predicted to coordinate with the Fe-S cluster and were shown to be essential for RirA repression of the sufS2-lacZ fusion. These results suggested that sufS2 is important for the survival of A. tumefaciens.

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Metal Homeostasis: Regulation of Manganese and Iron in the Rhizobia and Related α‐Proteobacteria

O’Brian

2004

Encyclopedia of Inorganic and Bioinorganic Chemistry

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Iron is required for many cellular processes, but can be toxic at high concentrations. Thus, iron homeostasis is strictly regulated so that iron acquisition, storage, and consumption are geared to iron availability, and that intracellular levels of free iron do not reach toxic levels. Recently, the roles of manganese and its control in cells have been investigated, and it is becoming clear that some aspects of the metabolism of iron and manganese are interrelated. Manganese is best understood in its role in oxidative stress responses, and the pro‐oxidative effects of intracellular iron functionally link these two metals. Iron and manganese appear to have complementary or compensatory functions as well. In bacteria, it may not be universally true that manganese is an essential nutrient under nonstressed conditions, underscoring a gap in our knowledge of the role of this metal in prokaryotes. Studies of Bradyrhizobium japonicum and other rhizobia reveal that control of iron‐responsive gene expression is fundamentally different in these bacteria when compared with model organisms such as Escherichia coli and Bacillus subtilis . Moreover, the Fur regulatory protein that dominates iron‐responsive gene expression in those model systems has been co‐opted to respond to manganese in the rhizobia. Finally, it appears that mechanisms of iron‐ and manganese‐responsive gene expression in the rhizobia are paradigmatic for the α‐proteobacteria. This is remarkable because the α‐proteobacteria are metabolically and ecologically diverse, making it difficult to correlate their unique metalloregulation with specific adaptations.

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The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability

Cited by 48 publications

References 58 publications

Antiparallel and Interlinked Control of Cellular Iron Levels by the Irr and RirA Regulators of Agrobacterium tumefaciens

Antiparallel and Interlinked Control of Cellular Iron Levels by the Irr and RirA Regulators of Agrobacterium tumefaciens

Cysteine desulphurase-encoding gene sufS2 is required for the repressor function of RirA and oxidative resistance in Agrobacterium tumefaciens

Metal Homeostasis: Regulation of Manganese and Iron in the Rhizobia and Related α‐Proteobacteria

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