Positive Control of Ferric Siderophore Receptor Gene Expression by the Irr Protein in<i>Bradyrhizobium japonicum</i>

Small, Sandra K.; Puri, Sumant; Sangwan, Indu; O’Brian, Mark R.

doi:10.1128/jb.01571-08

Cited by 42 publications

(81 citation statements)

References 31 publications

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“…2 A-C). In previous studies, we routinely cultured cells in media supplemented with trace elements that include manganese (15,17), and thus our observations agree with previous findings. However, those genes were not induced under iron limitation in cells grown in low-manganese media ( Fig.…”

Section: Resultssupporting

confidence: 91%

“…To further address the effects of manganese on iron metabolism, we examined the expression of several genes known to be regulated by iron at the mRNA level in B. japonicum wild-type cells. blr3555 and bll4920 encode iron siderophore transport outer-membrane receptors, and blr6519 encodes an iron-independent fumarase, which replaces the iron-sulfur fumarase when the metal is limiting (15,17,25). Cells were grown under various iron or manganese conditions, and mRNA encoding each gene was examined by quantitative realtime PCR (qPCR).…”

Section: Resultsmentioning

confidence: 99%

“…Thus, manganese contributes to the expression of these ironregulated genes, and further suggests that manganese affects irondependent metabolism. (15,17), and thus we wanted to address whether Irr expression or . mRNA transcripts of bll4920, blr3555, and blr6519 obtained from cells grown under different metal conditions were analyzed by qPCR.…”

Section: Resultsmentioning

confidence: 99%

“…In that case, B. japonicum would be less tolerant of iron when manganese is limiting. Irr positively controls iron transport genes (14,15,17), and an irr mutant is defective in iron uptake (18). Thus, diminution of Irr activity under manganese limitation will decrease iron acquisition.…”

Section: Discussionmentioning

confidence: 99%

“…Most genes that are strongly regulated by iron are directly or indirectly controlled by Irr (14,15). Irr functions under iron limitation, and binds to the promoters of target genes to positively or negatively regulate gene expression (14)(15)(16)(17). Positively controlled genes include those required for high-affinity iron transport, whereas many negatively regulated genes encode ironcontaining proteins.…”

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confidence: 99%

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Control of bacterial iron homeostasis by manganese

Puri

Hohle

O’Brian

2010

Proc. Natl. Acad. Sci. U.S.A.

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Perception and response to nutritional iron availability by bacteria are essential to control cellular iron homeostasis. The Irr protein from Bradyrhizobium japonicum senses iron through the status of heme biosynthesis to globally regulate iron-dependent gene expression. Heme binds directly to Irr to trigger its degradation. Here, we show that severe manganese limitation created by growth of a Mn 2+ transport mutant in manganese-limited media resulted in a cellular iron deficiency. In wild-type cells, Irr levels were attenuated under manganese limitation, resulting in reduced promoter occupancy of target genes and altered iron-dependent gene expression. Irr levels were high regardless of manganese availability in a heme-deficient mutant, indicating that manganese normally affects heme-dependent degradation of Irr. Manganese altered the secondary structure of Irr in vitro and inhibited binding of heme to the protein. We propose that manganese limitation destabilizes Irr under low-iron conditions by lowering the threshold of heme that can trigger Irr degradation. The findings implicate a mechanism for the control of iron homeostasis by manganese in a bacterium.Bradyrhizobium | heme | regulated degradation | oxidative stress

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Section: Resultssupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Control of bacterial iron homeostasis by manganese

Puri

Hohle

O’Brian

2010

Proc. Natl. Acad. Sci. U.S.A.

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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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Mechanisms and Regulation of Iron Homeostasis in the Rhizobia

Fabiano

O’Brian

2012

SpringerBriefs in Molecular Science

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Positive Control of Ferric Siderophore Receptor Gene Expression by the Irr Protein inBradyrhizobium japonicum

Cited by 42 publications

References 31 publications

Control of bacterial iron homeostasis by manganese

Control of bacterial iron homeostasis by manganese

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

Mechanisms and Regulation of Iron Homeostasis in the Rhizobia

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