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Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers.

Vinella D, Brochier-Armanet C, Loiseau L, Talla E, Barras F - PLoS Genet. (2009)

Bottom Line: Many bacteria contain multiple ATCs, as a result of gene duplication and/or horizontal gene transfer events.This model predicts the occurrence of a dynamic network, the structure and composition of which vary with the growth conditions.As an illustration, we depict three ways for a given protein to be matured, which appears to be dependent on the demand for Fe/S biogenesis.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Chimie Bactérienne, Institut Fédératif de Recherche 88, Institut de Microbiologie de la Méditerranée, Centre National de la Recherche Scientifique, Marseille, France.

ABSTRACT
Iron sulfur (Fe/S) proteins are ubiquitous and participate in multiple biological processes, from photosynthesis to DNA repair. Iron and sulfur are highly reactive chemical species, and the mechanisms allowing the multiprotein systems ISC and SUF to assist Fe/S cluster formation in vivo have attracted considerable attention. Here, A-Type components of these systems (ATCs for A-Type Carriers) are studied by phylogenomic and genetic analyses. ATCs that have emerged in the last common ancestor of bacteria were conserved in most bacteria and were acquired by eukaryotes and few archaea via horizontal gene transfers. Many bacteria contain multiple ATCs, as a result of gene duplication and/or horizontal gene transfer events. Based on evolutionary considerations, we could define three subfamilies: ATC-I, -II and -III. Escherichia coli, which has one ATC-I (ErpA) and two ATC-IIs (IscA and SufA), was used as a model to investigate functional redundancy between ATCs in vivo. Genetic analyses revealed that, under aerobiosis, E. coli IscA and SufA are functionally redundant carriers, as both are potentially able to receive an Fe/S cluster from IscU or the SufBCD complex and transfer it to ErpA. In contrast, under anaerobiosis, redundancy occurs between ErpA and IscA, which are both potentially able to receive Fe/S clusters from IscU and transfer them to an apotarget. Our combined phylogenomic and genetic study indicates that ATCs play a crucial role in conveying ready-made Fe/S clusters from components of the biogenesis systems to apotargets. We propose a model wherein the conserved biochemical function of ATCs provides multiple paths for supplying Fe/S clusters to apotargets. This model predicts the occurrence of a dynamic network, the structure and composition of which vary with the growth conditions. As an illustration, we depict three ways for a given protein to be matured, which appears to be dependent on the demand for Fe/S biogenesis.

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Model for Fe/S trafficking leading to IspG/H maturation in E. coli.Diagram depicted in panel (A) shows all possible Fe/S paths deduced from the present study and from the current literature. Path 1 was deduced from the observation that sufA acts as a multicopy suppressor of the iscUA erpA strain in a sufB-dependent manner and from in vitro studies ([48] and Fontecave's group personal communication). Path 2 was deduced from the viabilities of the iscA sufB, iscA sufCD and iscU sufA mutants. Path 3 was deduced from the observations that (i) erpA acts as a multicopy suppressor of the iscA sufA mutant in an iscU-dependent manner; (ii) the sufA iscA mutant is viable under anaerobiosis only in the presence of functional copies of iscU and erpA. Path 4 was deduced from the anaerobic-dependent growth of the Δsuf erpA mutant. Path 5 was deduced from the observation that sufA acts as a multicopy suppressor of iscUA erpA. Path 6 was deduced from the identity between the phenotypes of the iscA sufA and erpA mutants and phylogenomic analysis; other interpretations are that: (i) ErpA acts between the IscU/SufBCD and the IscA/SufA components; (ii) IscA, SufA and ErpA interact to build a heteromeric complex. Path 7 was deduced from the observation that multicopy erpA suppresses the iscA sufA conditional lethal phenotype. Diagrams depicted in panels (B), (C), (D) represent models for IspG/H maturation under different growth conditions as indicated under each panel. The situations depicted make use of a minimum number of Fe/S biogenesis components and are meant for describing a cell expressing the Fe/S biogenesis genes involved at their physiological level.
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pgen-1000497-g003: Model for Fe/S trafficking leading to IspG/H maturation in E. coli.Diagram depicted in panel (A) shows all possible Fe/S paths deduced from the present study and from the current literature. Path 1 was deduced from the observation that sufA acts as a multicopy suppressor of the iscUA erpA strain in a sufB-dependent manner and from in vitro studies ([48] and Fontecave's group personal communication). Path 2 was deduced from the viabilities of the iscA sufB, iscA sufCD and iscU sufA mutants. Path 3 was deduced from the observations that (i) erpA acts as a multicopy suppressor of the iscA sufA mutant in an iscU-dependent manner; (ii) the sufA iscA mutant is viable under anaerobiosis only in the presence of functional copies of iscU and erpA. Path 4 was deduced from the anaerobic-dependent growth of the Δsuf erpA mutant. Path 5 was deduced from the observation that sufA acts as a multicopy suppressor of iscUA erpA. Path 6 was deduced from the identity between the phenotypes of the iscA sufA and erpA mutants and phylogenomic analysis; other interpretations are that: (i) ErpA acts between the IscU/SufBCD and the IscA/SufA components; (ii) IscA, SufA and ErpA interact to build a heteromeric complex. Path 7 was deduced from the observation that multicopy erpA suppresses the iscA sufA conditional lethal phenotype. Diagrams depicted in panels (B), (C), (D) represent models for IspG/H maturation under different growth conditions as indicated under each panel. The situations depicted make use of a minimum number of Fe/S biogenesis components and are meant for describing a cell expressing the Fe/S biogenesis genes involved at their physiological level.

Mentions: Because the inactivation of the ispG or the ispH gene is lethal in anaerobiosis, these results showed that ErpA and IscA were both able to ensure enough IspG/H maturation to produce sufficient IPP to sustain growth (Paths 4 and 7 in Figure 3A). Thus, ErpA and IscA are redundant under anaerobiosis.


Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers.

Vinella D, Brochier-Armanet C, Loiseau L, Talla E, Barras F - PLoS Genet. (2009)

Model for Fe/S trafficking leading to IspG/H maturation in E. coli.Diagram depicted in panel (A) shows all possible Fe/S paths deduced from the present study and from the current literature. Path 1 was deduced from the observation that sufA acts as a multicopy suppressor of the iscUA erpA strain in a sufB-dependent manner and from in vitro studies ([48] and Fontecave's group personal communication). Path 2 was deduced from the viabilities of the iscA sufB, iscA sufCD and iscU sufA mutants. Path 3 was deduced from the observations that (i) erpA acts as a multicopy suppressor of the iscA sufA mutant in an iscU-dependent manner; (ii) the sufA iscA mutant is viable under anaerobiosis only in the presence of functional copies of iscU and erpA. Path 4 was deduced from the anaerobic-dependent growth of the Δsuf erpA mutant. Path 5 was deduced from the observation that sufA acts as a multicopy suppressor of iscUA erpA. Path 6 was deduced from the identity between the phenotypes of the iscA sufA and erpA mutants and phylogenomic analysis; other interpretations are that: (i) ErpA acts between the IscU/SufBCD and the IscA/SufA components; (ii) IscA, SufA and ErpA interact to build a heteromeric complex. Path 7 was deduced from the observation that multicopy erpA suppresses the iscA sufA conditional lethal phenotype. Diagrams depicted in panels (B), (C), (D) represent models for IspG/H maturation under different growth conditions as indicated under each panel. The situations depicted make use of a minimum number of Fe/S biogenesis components and are meant for describing a cell expressing the Fe/S biogenesis genes involved at their physiological level.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2682760&req=5

pgen-1000497-g003: Model for Fe/S trafficking leading to IspG/H maturation in E. coli.Diagram depicted in panel (A) shows all possible Fe/S paths deduced from the present study and from the current literature. Path 1 was deduced from the observation that sufA acts as a multicopy suppressor of the iscUA erpA strain in a sufB-dependent manner and from in vitro studies ([48] and Fontecave's group personal communication). Path 2 was deduced from the viabilities of the iscA sufB, iscA sufCD and iscU sufA mutants. Path 3 was deduced from the observations that (i) erpA acts as a multicopy suppressor of the iscA sufA mutant in an iscU-dependent manner; (ii) the sufA iscA mutant is viable under anaerobiosis only in the presence of functional copies of iscU and erpA. Path 4 was deduced from the anaerobic-dependent growth of the Δsuf erpA mutant. Path 5 was deduced from the observation that sufA acts as a multicopy suppressor of iscUA erpA. Path 6 was deduced from the identity between the phenotypes of the iscA sufA and erpA mutants and phylogenomic analysis; other interpretations are that: (i) ErpA acts between the IscU/SufBCD and the IscA/SufA components; (ii) IscA, SufA and ErpA interact to build a heteromeric complex. Path 7 was deduced from the observation that multicopy erpA suppresses the iscA sufA conditional lethal phenotype. Diagrams depicted in panels (B), (C), (D) represent models for IspG/H maturation under different growth conditions as indicated under each panel. The situations depicted make use of a minimum number of Fe/S biogenesis components and are meant for describing a cell expressing the Fe/S biogenesis genes involved at their physiological level.
Mentions: Because the inactivation of the ispG or the ispH gene is lethal in anaerobiosis, these results showed that ErpA and IscA were both able to ensure enough IspG/H maturation to produce sufficient IPP to sustain growth (Paths 4 and 7 in Figure 3A). Thus, ErpA and IscA are redundant under anaerobiosis.

Bottom Line: Many bacteria contain multiple ATCs, as a result of gene duplication and/or horizontal gene transfer events.This model predicts the occurrence of a dynamic network, the structure and composition of which vary with the growth conditions.As an illustration, we depict three ways for a given protein to be matured, which appears to be dependent on the demand for Fe/S biogenesis.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire de Chimie Bactérienne, Institut Fédératif de Recherche 88, Institut de Microbiologie de la Méditerranée, Centre National de la Recherche Scientifique, Marseille, France.

ABSTRACT
Iron sulfur (Fe/S) proteins are ubiquitous and participate in multiple biological processes, from photosynthesis to DNA repair. Iron and sulfur are highly reactive chemical species, and the mechanisms allowing the multiprotein systems ISC and SUF to assist Fe/S cluster formation in vivo have attracted considerable attention. Here, A-Type components of these systems (ATCs for A-Type Carriers) are studied by phylogenomic and genetic analyses. ATCs that have emerged in the last common ancestor of bacteria were conserved in most bacteria and were acquired by eukaryotes and few archaea via horizontal gene transfers. Many bacteria contain multiple ATCs, as a result of gene duplication and/or horizontal gene transfer events. Based on evolutionary considerations, we could define three subfamilies: ATC-I, -II and -III. Escherichia coli, which has one ATC-I (ErpA) and two ATC-IIs (IscA and SufA), was used as a model to investigate functional redundancy between ATCs in vivo. Genetic analyses revealed that, under aerobiosis, E. coli IscA and SufA are functionally redundant carriers, as both are potentially able to receive an Fe/S cluster from IscU or the SufBCD complex and transfer it to ErpA. In contrast, under anaerobiosis, redundancy occurs between ErpA and IscA, which are both potentially able to receive Fe/S clusters from IscU and transfer them to an apotarget. Our combined phylogenomic and genetic study indicates that ATCs play a crucial role in conveying ready-made Fe/S clusters from components of the biogenesis systems to apotargets. We propose a model wherein the conserved biochemical function of ATCs provides multiple paths for supplying Fe/S clusters to apotargets. This model predicts the occurrence of a dynamic network, the structure and composition of which vary with the growth conditions. As an illustration, we depict three ways for a given protein to be matured, which appears to be dependent on the demand for Fe/S biogenesis.

Show MeSH
Related in: MedlinePlus