SufA from Erwinia chrysanthemi

SufA is a component of the recently discoveredsuf operon, which has been shown to play an important function in bacteria during iron-sulfur cluster biosynthesis and resistance to oxidative stress. The SufA protein from Erwinia chrysanthemi, a Gram-negative plant pathogen, has been purified to homogeneity and characterized. It is a homodimer with the ability to assemble rather labile [2Fe-2S] and [4Fe-4S] clusters as shown by Mössbauer spectroscopy. These clusters can be transferred to apoproteins such as ferredoxin or biotin synthase during a reaction that is not inhibited by bathophenanthroline, an iron chelator. Cluster assembly in these proteins is much more efficient when iron and sulfur are provided by holoSufA than by free iron sulfate and sodium sulfide. We propose the function of SufA is that of a scaffold protein for [Fe-S] cluster assembly and compare it to IscA, a member of theisc operon also involved in cluster biosynthesis in both prokaryotes and eukaryotes. Mechanistic and physiological implications of these results are also discussed. SufA is a component of the recently discoveredsuf operon, which has been shown to play an important function in bacteria during iron-sulfur cluster biosynthesis and resistance to oxidative stress. The SufA protein from Erwinia chrysanthemi, a Gram-negative plant pathogen, has been purified to homogeneity and characterized. It is a homodimer with the ability to assemble rather labile [2Fe-2S] and [4Fe-4S] clusters as shown by Mössbauer spectroscopy. These clusters can be transferred to apoproteins such as ferredoxin or biotin synthase during a reaction that is not inhibited by bathophenanthroline, an iron chelator. Cluster assembly in these proteins is much more efficient when iron and sulfur are provided by holoSufA than by free iron sulfate and sodium sulfide. We propose the function of SufA is that of a scaffold protein for [Fe-S] cluster assembly and compare it to IscA, a member of theisc operon also involved in cluster biosynthesis in both prokaryotes and eukaryotes. Mechanistic and physiological implications of these results are also discussed. iron-sulfur cluster dithiothreitol biotin synthase ferredoxin iron-sulfur cluster pyridoxal 5-phosphate bathophenanthroline disulfonate deazaflavin vesicular somatidis virus-glycoprotein nickel-nitrilotriacetic acid Iron-sulfur [Fe-S] proteins play important roles in electron transfer, in redox and non-redox catalysis, in regulation, and as sensors within all living organisms, prokaryotes and eukaryotes (1Beinert H. Holm R.H. Münck E. Science. 1997; 277: 653-659Crossref PubMed Scopus (1530) Google Scholar, 2Beinert H. J. Biol. Inorg. Chem. 2000; 5: 2-15Crossref PubMed Scopus (538) Google Scholar). The biosynthetic process by which defined proportions of iron and sulfur atoms are mobilized from their storage sources and combined in a controlled way to generate the various iron-sulfur cluster prosthetic groups is still far from understood. It requires a complex protein machinery that is only now becoming identified and characterized. In the bacteria Escherichia coli and Azotobacter vinelandii, from which most of the available information is derived, this machinery has been found to be encoded by a highly conserved cluster of at least seven genes,iscRSUA-hscBA-fdx, also named the ISC1 (foriron-sulfur cluster) machinery (3Zheng L. Cash V.L. Flint D.H. Dean D.R. J. Biol. Chem. 1998; 273: 13264-13272Abstract Full Text Full Text PDF PubMed Scopus (575) Google Scholar,4Frazzon J. Dean D.R. Proc. Natl. Acad. Sci. U. S. A. 2001; 98: 14751-14753Crossref PubMed Scopus (29) Google Scholar). 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PubMed Scopus Google Scholar, H. Biol. 2000; PubMed Scopus Google Scholar, H. J. Proc. Natl. Acad. Sci. U. S. A. 2001; 98: PubMed Scopus Google Scholar, J. Biol. 2001; PubMed Scopus Google Scholar). proteins are that the of sulfur from for clusters D.H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, L. R.H. Cash V.L. Dean D.R. PubMed Scopus Google Scholar). and proteins are to assemble and labile [2Fe-2S] and [4Fe-4S] as shown by Mössbauer and S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Dean D.R. 2000; PubMed Scopus Google Scholar, L. Cash V.L. Dean D.R. J. Chem. 2000; Scopus Google Scholar, J. Dean D.R. 2001; PubMed Scopus Google Scholar, J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar, PubMed Scopus Google Scholar, J. Biol. Inorg. Chem. PubMed Scopus Google Scholar, S. PubMed Scopus Google Scholar, S. PubMed Scopus Google Scholar). 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Chem. 2000; Scopus Google Scholar, S. H. U. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Dean D.R. J. Chem. 2001; PubMed Scopus Google Scholar). both and can with the of of the machinery S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Biol. Inorg. Chem. PubMed Scopus Google Scholar, S. PubMed Scopus Google Scholar). is a [2Fe-2S] that electron are of the cluster assembly process J. Biol. Chem. Full Text PDF PubMed Google Scholar). all of these proteins been in and the by which to an [Fe-S] cluster an is not and is the of in of to this important the of the protein from E. coli S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). are many for it is important to most both and with It is generally that proteins are the in the cluster assembly is for In to this is the in a of both is whereas a of both and only results in of iron in and in the of and [Fe-S] enzymes U. 2000; PubMed Scopus Google Scholar, Biol. 2000; PubMed Scopus Google Scholar, J. Biol. PubMed Scopus Google Scholar, A. H. J. Biol. Chem. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar). the it recently an in [Fe-S] cluster assembly that from S. in decreased during cluster assembly in biotin a [4Fe-4S] when with U. J. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar). for the of proteins is the of an operon in bacteria and also involved in iron and sulfur operon an and J. PubMed Google Scholar, 2001; PubMed Scopus Google Scholar, U. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar). In to S. the genes of theisc operon are for are not for the of E. coli In an E. coli in which the operon has been the activity of [Fe-S] proteins is only of their activity in U. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar). is to the of the genes as by the that overexpression of operon the and activity of [Fe-S] proteins in the all of the when both the and U. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar). Erwinia chrysanthemi, a Gram-negative plant pathogen, and E. recently provided more information the In both the operon found to be the in E. coli at it also found to to the oxidative D.R. J. 2001; PubMed Scopus Google Scholar, L. L. 2001; PubMed Scopus Google Scholar, J. Google Scholar). a function of the machinery during of [Fe-S] clusters as a of oxidative and a iron to be the most protein in this of in E. in decreased increased of free iron increased to oxidative of the of the by a [2Fe-2S] of enzymes labile [Fe-S] oxidative and decreased of E. J. PubMed Google Scholar, L. L. 2001; PubMed Scopus Google Scholar, L. L. J. PubMed Scopus Google Scholar). iron shown to be a of a decreased ability to iron from such as or [Fe-S] clusters in are not in this J. PubMed Google Scholar, L. L. 2001; PubMed Scopus Google Scholar, L. L. J. PubMed Scopus Google Scholar). the of the proteins been at the far H. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar, H. J. PubMed Scopus Google Scholar, J. Biol. PubMed Scopus Google Scholar). this a to of [Fe-S] cluster it is than the it not of the ferredoxin protein and of the and by the of an whereas a protein to is of the an to the function of an the acid of SufA proteins from a of and with proteins is SufA and from the E. In the of IscA, which been shown by in the of the protein to be for function and to be involved in iron are in SufA proteins Biol. 2000; PubMed Scopus Google Scholar, A. H. J. Biol. Chem. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar). It is to that SufA has the to assemble an [Fe-S] cluster and to in a way to IscA, as a scaffold for [Fe-S] cluster assembly in this protein the only protein that with is a which to the the operon proteins that are not in cluster of The available that and which are encoded by highly conserved genes in and to a complex with activity L. L. J. PubMed Scopus Google Scholar). 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Münck E. 2000; PubMed Scopus Google Scholar, S. E. PubMed Scopus Google Scholar). an [2Fe-2S] cluster and not and 2001; PubMed Scopus Google Scholar, 2001; PubMed Scopus Google Scholar). it is important to and for both not the production of more than of biotin of S. E. PubMed Scopus Google Scholar, 2001; PubMed Scopus Google Scholar, S. E. PubMed Scopus Google Scholar). In the the of the [4Fe-4S] cluster of the the with of only a of iron and in the of Cluster from SufA to by the for biotin synthase in this it is that these reaction only the of and that the reaction the biotin synthase activity of of of In activity when with of iron and with or also the results from E. coli as an [Fe-S] cluster during cluster to These that SufA and are efficient for of as S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). a for the of the found that iron-sulfur clusters from the [4Fe-4S] protein of the J. E. A. J. Biol. Chem. 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Full Text PDF PubMed Google not be transferred to Iron-sulfur cluster assembly can a and of the cluster from holoSufA to the or an with a and of the cluster in the a of free iron and by the and assembly of the the by which the cluster reaction the of a free iron that it not activity and not iron from SufA or at not to be an of the cluster reaction only in the of an which that iron and holoSufA at with of and biotin synthase activity a shown in not the iron-sulfur cluster from holoSufA to the reaction in the or in the of of the iron chelator. the of the cluster of biotin synthase during of with of iron and inhibited by of Cluster also with in the of with and that not during the [Fe-S] process rather for of in the of the of acid with a protein of the operon shown to be to assemble an iron-sulfur the that of the of the also the to is now shown for the with a purified of the SufA protein from E. and of both and proteins as as and Mössbauer are with the of iron-sulfur clusters in this are many and SufA These are in the both purified proteins are found in the with to and SufA proteins in conserved and for SufA from E. chrysanthemi, of by acid has been for an from In this has shown that these are to in the [2Fe-2S] cluster J. Science. PubMed Scopus Google Scholar). In the of and from the S. these been to function as for acid for of the the as Biol. 2000; PubMed Scopus Google A. H. J. Biol. Chem. 2000; Full Text Full Text PDF PubMed Scopus Google Scholar). as the proteins not been purified and characterized. the in the of from the proteins in and found to be to a cluster the in for the protein J. Biol. Inorg. Chem. PubMed Scopus Google Scholar). These clusters and Mössbauer to of the the of the clusters of the proteins found to be with to that of the these results not an that these conserved are at the such an and that play an function in this be by It is important to that not only is in also conserved and are as and be in least of these the to a cluster by the clusters in SufA from E. are and are during to the protein in the the protein also cluster during with oxidative and of SufA clusters also in the of from E. coli or Azotobacter and from S. S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Dean D.R. 2001; PubMed Scopus Google Scholar, J. Biol. Inorg. Chem. PubMed Scopus Google Scholar). It be in both SufA and IscA, iron is to the protein only in the of sulfide. These proteins are not in only iron the SufA protein can to iron and sulfur atoms within both with Mössbauer and the [2Fe-2S] clusters are the way to the [4Fe-4S] or are of labile [4Fe-4S] clusters to be all of with of both and as shown by Mössbauer to the in to the for an efficient of clusters in proteins from various been shown to the of iron and sulfur atoms during of the S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google J. Dean D.R. 2001; PubMed Scopus Google Scholar, J. Biol. Inorg. Chem. PubMed Scopus Google Scholar). the results been in the the of clusters in proteins S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Dean D.R. 2001; PubMed Scopus Google Scholar, J. Biol. Inorg. Chem. PubMed Scopus Google Scholar). of the protein from E. coli by to the of the of [2Fe-2S] clusters S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). this is not as efficient for of [4Fe-4S] clusters in and not the that [4Fe-4S] clusters are also in E. coli Mössbauer which is the to [2Fe-2S] and [4Fe-4S] has not been to this Mössbauer has been to the clusters in from S. and from A. J. Dean D.R. 2001; PubMed Scopus Google Scholar, J. Biol. Inorg. Chem. PubMed Scopus Google Scholar). In the only [2Fe-2S] clusters be with Mössbauer and J. Biol. Inorg. Chem. PubMed Scopus Google Scholar). the in the of from A. vinelandii, a of the during with free iron and provided by that the protein can assemble both [2Fe-2S] and [4Fe-4S] with Mössbauer to of the clusters of SufA for [2Fe-2S] and for J. Dean D.R. 2001; PubMed Scopus Google Scholar). The [2Fe-2S] clusters been shown to be during the cluster assembly the [4Fe-4S] clusters shown to be their of the is at the of the the this also be an of these proteins in to their as sources of clusters during [Fe-S] assembly in apoproteins a more of the iron in both and SufA a of the that to be both SufA and are at least in to iron and atoms to S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). The that ferredoxin can iron and sulfur not only from [2Fe-2S] and [4Fe-4S] clusters in SufA also from These a of iron and sulfur in as shown by Mössbauer spectroscopy. The of the [2Fe-2S] cluster of ferredoxin is when iron and sulfur are in SufA when as when are provided in the of free iron and is with the that SufA the of a scaffold protein for assembly of [Fe-S] a for sulfur and iron function not be a of the proteins and proteins also to play this S. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J. Biol. 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In this that SufA not only as a [2Fe-2S] cluster to as also as a [4Fe-4S] for biotin In this also cluster at a when iron and sulfur atoms provided by holoSufA as with free iron and sulfide. that both holoSufA and can their clusters to a protein can both of clusters to proteins a can clusters from scaffold These in results to the that the [Fe-S] cluster assembly process of cluster and the of are the and the the to of the and in bacteria or and in the the and a complex and as an a for during cluster and that to this L. L. J. PubMed Scopus Google Scholar). also has a function is a that to be The is the in the of an electron protein such as In ferredoxin and ferredoxin are of the [Fe-S] cluster their H. A. Proc. Natl. Acad. Sci. U. S. A. 2000; PubMed Scopus Google Scholar, J. S. A. J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, L. 1998; PubMed Scopus Google Scholar). for a redox in this biosynthetic is not be for and of iron from storage or of assembly of the cluster and of the [Fe-S] cluster from with a scaffold the not and by a or it that to be We that is an to it a of for assembly of [Fe-S] clusters and the for that In propose a for [Fe-S] cluster In this SufA as a scaffold protein iron and sulfur atoms in with to generate sulfur from The of iron is still in the not for cluster from it is in shown the of this protein complex during [Fe-S] cluster assembly U. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google Scholar, L. L. 2001; PubMed Scopus Google Scholar, L. L. J. PubMed Scopus Google Scholar). has an cluster assembly in SufA or cluster in to be It be to that the of the proteins is still a of found in the in E. coli and in the in coli and E. 2001; PubMed Scopus Google L. L. 2001; PubMed Scopus Google Scholar). L. L. and that all proteins the that SufA found to be in the in the the In electron is as that a not encoded by the operon in the which are to be the most that it is to with These in their only proteins of the and and ferredoxin 2001; PubMed Scopus Google Scholar). a of the of cluster from holoSufA to results that this is not a with a of iron and sulfur atoms from holoSufA in by their by the is more with the of with free iron and as with holoSufA and the of of bathophenanthroline, a the In the cluster by free iron and sulfur is inhibited by this chelator. The of a process is the for scaffold proteins for assembly of [Fe-S] clusters in In a cluster be SufA the way to this cluster be to the We are in the of the cluster this requires a of cluster assembly in which is Cluster assembly in biotin synthase the of has also been in from S. U. J. J. Biol. Chem. 277: Full Text Full Text PDF PubMed Scopus Google shown that and of is the of and is the of whereas is the electron in with the for ferredoxin electron The for is with the that are involved in cluster The of has been the that be in the and that be for as a for not results that is not during cluster from SufA to has been with and The most in this of in the of and SufA is that a in a in [Fe-S] In of in only with the that are proteins or in the of proteins and a during [Fe-S] cluster as a scaffold protein for [Fe-S] cluster assembly and to