Highlighted Text:
Show |
Hide
Full text loading...
Chapter 30 : Mechanisms and Regulation of Iron Uptake in the Rhizobia
Author:
Andrew W. B. Johnston1
VIEW AFFILIATIONS
HIDE AFFILIATIONS
Affiliations:
1: School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom
Content Type: Monograph
Publication Year:
2004
Category: Bacterial Pathogenesis; Clinical Microbiology
Book DOI:
10.1128/9781555816544
Chapter DOI:
10.1128/9781555816544.ch30
MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Preview this chapter:
Mechanisms and Regulation of Iron Uptake in the Rhizobia, Page 1 of 2
< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555816544/9781555812928_Chap30-1.gif /docserver/preview/fulltext/10.1128/9781555816544/9781555812928_Chap30-2.gif
Abstract:
This chapter considers only recent experimental and in silico analyses that directly apply to the iron biology of rhizobia. At least two main sets of observations have emerged from these studies and are recurring themes in the chapter. The first is that the rhizobia have great flexibility in their use of iron sources compared to many other bacteria. The second is that some paradigms of iron-responsive gene regulation do not operate in the rhizobia or, at least, not all rhizobia. There have been detailed biochemical and genetic studies of only two rhizobial siderophores. These are the trihydroxamate vicibactin (VB), made by most strains of Rhizobium leguminosarum, and the chemically distinct dihydroxamate rhizobactin 1021 (RB1021), synthesized by different strains of S. meliloti, including the well-characterized strain 1021—hence the name RB1021. The expression of bacterial genes involved in iron uptake and other aspects of “iron biology” responds to iron availability, and the rhizobia are no exception. It is clear that the rhizobia have great flexibility for iron uptake and show real differences in their iron-responsive gene regulation compared to other gram-negative bacteria. Importantly, it is now evident that as much as 50% of the genome of one rhizobial species does not resemble those of other, even closely related species (e.g., Sinorhizobium meliloti and R. leguminosarum). Focusing on mechanisms of iron uptake, these lines of argument may explain why rhizobia not only use siderophores but also contain at least two transport systems more frequently associated with pathogens.
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
Figures
Mechanisms and Regulation of Iron Uptake in the Rhizobia
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816544.chap30-1,webId=/content/author/10.1128/9781555816544.chap30-1,properties={foaf_givenname=Andrew W. B., foaf_name=Andrew W. B. Johnston, foaf_surname=Johnston, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816544.chap30-aff1]]}]]
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.fig30-1
FIGURE 1
Structures of three chemically characterized siderophores made by rhizobia.
10.1128/9781555816544/fig30-1_thmb.gif
10.1128/9781555816544/fig30-1.gif
FIGURE 1
Structures of three chemically characterized siderophores made by rhizobia.
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.fig30-2
FIGURE 2
Organization of gene clusters involved in siderophore synthesis and uptake in R. leguminosarum and S. meliloti. Relative locations of genes for the synthesis and uptake of the siderophores VB by R. leguminosarum (a) and RB1021 by S. meliloti (b) are shown. Dotted lines indicate transcriptional organization of the different operons. Gene functions are given in the text, Table 2 , and Fig. 3 and 4 . Data from Carter et al. (2002) for VB and from Lynch et al. (2001) for RB1021.
10.1128/9781555816544/fig30-2_thmb.gif
10.1128/9781555816544/fig30-2.gif
FIGURE 2
Organization of gene clusters involved in siderophore synthesis and uptake in R. leguminosarum and S. meliloti. Relative locations of genes for the synthesis and uptake of the siderophores VB by R. leguminosarum (a) and RB1021 by S. meliloti (b) are shown. Dotted lines indicate transcriptional organization of the different operons. Gene functions are given in the text, Table 2 , and Fig. 3 and 4 . Data from Carter et al. (2002) for VB and from Lynch et al. (2001) for RB1021.
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.fig30-3
FIGURE 3
Pathway of VB synthesis. The proposed pathway for VB synthesis in R. leguminosarum is shown. The numbered steps correspond to those in Table 2 . Adapted from Carter et al. (2002) .
10.1128/9781555816544/fig30-3_thmb.gif
10.1128/9781555816544/fig30-3.gif
FIGURE 3
Pathway of VB synthesis. The proposed pathway for VB synthesis in R. leguminosarum is shown. The numbered steps correspond to those in Table 2 . Adapted from Carter et al. (2002) .
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.fig30-4
FIGURE 4
Pathway of RB1021 synthesis. The proposed pathway for RB1021 synthesis in S. meliloti is shown. Adapted from Lynch et al. (2001) .
10.1128/9781555816544/fig30-4_thmb.gif
10.1128/9781555816544/fig30-4.gif
FIGURE 4
Pathway of RB1021 synthesis. The proposed pathway for RB1021 synthesis in S. meliloti is shown. Adapted from Lynch et al. (2001) .
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.fig30-5
FIGURE 5
Phylogenic tree of the Fur superfamily in the rhizobia, compared with homologues in other bacterial taxa. A maximum-parsimony phylogenetic tree was constructed from amino acid sequences of Fur and Fur-like sequences by using PAUP* version 4.0b10. The tree is rooted at the midpoints, and bootstrap values are shown for nodes with values of >70. Branch lengths are proportional to the degree of amino acid change. Proteins were obtained from the GenBank database. A.ae, Aquifex aeolicus; A.tum, Agrobacterium tumefaciens; B.jap, Bradyrhizobium japonicum; B.sub, Bacillus subtilis; B.hen, Bartonella henselae; B.mel, Brucella melintensis; B.per, Bordetella pertussis; C.ac, Clostridium acetobutylicum; C.cre, Caulobacter crescentus; D.vu, Desulfovibrio vulgaris; E.col, Escherichia coli K-12; H.inf, Haemophilus influenzae; H.pyl, Helicobacter pylori; K.pne, Klebsiella pneumoniae; L.pne, Legionella pneumophila; L.inn, Listeria innocua; M.lot, Mesorhizobium loti; N.men, Neisseria meningitidis; P.aer, Pseudomonas aeruginosa; P.mul, Pasteurella multocida; R.leg, Rhizobium leguminosarum, R.sph, Rhodobacter sphaeroides; R.pa, Rhodopseudomonas palustris; S.ent, Salmonella enterica; S.mel, Sinorhizobium meliloti, S.typ, Salmonella enterica serovar Typhimurium; S.aur, Staphylococcus aureus; T.mar, Thermotoga maritima; V.ang, Vibrio anguillarum; V.cho, Vibrio cholerae; Y.pes, Yersinia pestis. Proteins from Agrobacterium, Brucella, Mesorhizobium, Rhizobium, and Sinorhizobium are marked with stars.
10.1128/9781555816544/fig30-5_thmb.gif
10.1128/9781555816544/fig30-5.gif
FIGURE 5
Phylogenic tree of the Fur superfamily in the rhizobia, compared with homologues in other bacterial taxa. A maximum-parsimony phylogenetic tree was constructed from amino acid sequences of Fur and Fur-like sequences by using PAUP* version 4.0b10. The tree is rooted at the midpoints, and bootstrap values are shown for nodes with values of >70. Branch lengths are proportional to the degree of amino acid change. Proteins were obtained from the GenBank database. A.ae, Aquifex aeolicus; A.tum, Agrobacterium tumefaciens; B.jap, Bradyrhizobium japonicum; B.sub, Bacillus subtilis; B.hen, Bartonella henselae; B.mel, Brucella melintensis; B.per, Bordetella pertussis; C.ac, Clostridium acetobutylicum; C.cre, Caulobacter crescentus; D.vu, Desulfovibrio vulgaris; E.col, Escherichia coli K-12; H.inf, Haemophilus influenzae; H.pyl, Helicobacter pylori; K.pne, Klebsiella pneumoniae; L.pne, Legionella pneumophila; L.inn, Listeria innocua; M.lot, Mesorhizobium loti; N.men, Neisseria meningitidis; P.aer, Pseudomonas aeruginosa; P.mul, Pasteurella multocida; R.leg, Rhizobium leguminosarum, R.sph, Rhodobacter sphaeroides; R.pa, Rhodopseudomonas palustris; S.ent, Salmonella enterica; S.mel, Sinorhizobium meliloti, S.typ, Salmonella enterica serovar Typhimurium; S.aur, Staphylococcus aureus; T.mar, Thermotoga maritima; V.ang, Vibrio anguillarum; V.cho, Vibrio cholerae; Y.pes, Yersinia pestis. Proteins from Agrobacterium, Brucella, Mesorhizobium, Rhizobium, and Sinorhizobium are marked with stars.
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
References
/content/book/10.1128/9781555816544.chap30
1.
Carter, R. A.,, P. S. Worsley,, G. Sawers,, G. L. Challis,, M. J. Dilworth,, K. C. Carson,, J. A. Lawrence,, M. Wexler,, A. W. B. Johnston,, and K. H. Yeoman. 2002. The vbs genes that direct synthesis of the siderophore vicibactin in Rhizobium leguminosarum: their expression in other genera requires ECF σ factor RpoI. Mol. Microbiol. 44: 1153– 1166.
2.
Dilworth, M. J.,, K. C. Carson,, R. G. F. Giles,, L. T. Byrne,, and A. R. Glenn. 1998. Rhizobium leguminosarum bv. viciae produces a novel cyclic trihydroxamate siderophore, vicibactin. Microbiology 144: 781– 791.
3.
Hamza, I.,, S. Chauhan,, R. Hassett,, and M. R. O’Brian. 1998. The bacterial Irr protein is required for coordination of heme biosynthesis with iron availability. J. Biol. Chem. 273: 21669– 21674.
4.
Hamza, I.,, R. Hassett,, and M. R. O’Brian. 1999. Identification of a functional fur gene in Bradyrhizobium japonicum. J. Bacterol. 181: 5843– 5846.
5.
Hamza, I.,, Z. H. Qi,, N. D. King,, and M. R. O’Brian. 2000. Fur-independent regulation of iron metabolism by Irr in Bradyrhizobium japonicum. Microbiology 146: 669– 676.
6.
Hirsch, A. M.,, M. R. Lum,, and J. A. Downie. 2001. What makes the rhizobia-legume symbiosis so special? Plant Physiol. 127: 1484– 1492.
7.
Johnston, A. W. B.,, K. H. Yeoman,, and M. Wexler. 2001. Metals and the rhizobial-legume symbiosis— uptake, utilization and signalling. Adv. Microb. Physiol. 45: 114– 156.
8.
Kolade O. O.,, P. Bellini,, M. Wexler,, A. W. B. Johnston,, J. G. Grossmann,, and A. M. Hemmings. 2002. Structural studies of the Fur protein from Rhizobium leguminosarum. Biochem. Soc. Trans. 30: 771– 774.
9.
LeVier, K.,, D. A. Day,, and M. L. Guerinot. 1996. Iron uptake by symbiosomes from soybean nodules. Plant Physiol. 111: 893– 900.
10.
LeVier, K.,, and M. L. Guerinot. 1996. The Bradyrhizobium japonicum fegA gene encodes an iron-regulated membrane protein with similarity to hydroxamate- type siderophore receptors. J. Bacteriol. 178: 7265– 7275.
11.
Lynch, D.,, J. O’Brien,, T. Welch,, J. H. Crosa,, and M. O’Connell. 2001. Genetic organization of the region encoding regulation, biosynthesis and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J. Bacteriol. 183: 2576– 2585.
12.
Moreau, S.,, D. A. Day,, and A. Puppo. 1998. Ferrous iron is transported across the peribacteroid membrane of soybean nodules. Planta 207: 83– 87.
13.
Nienaber, A.,, H. Hennecke,, and H. M. Fischer. 2001. Discovery of a haem uptake system in the soil bacterium Bradyrhizobium japonicum. Mol. Microbiol. 41: 787– 800.
14.
Noya, F.,, A. Arias,, and E. Fabiano. 1997. Heme compounds as iron sources for nonpathogenic Rhizobium species. J. Bacteriol. 179: 3076– 3078.
15.
Platero, R. A.,, M. Jaureguy,, F. J. Battistoni,, and E. R. Fabiano. 2003. Mutations in sitB and sitD genes affect manganese-growth requirements in Sinorhizobium meliloti. FEMS Microbiol. Lett. 218: 65– 70.
16.
Pohl, E.,, J. C. Haller,, A. Mijovilovich,, W. Meyer- Klaucke,, E. Garman,, and M. L. Vasil. 2003. Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol. Microbiol. 47: 903– 915.
17.
Qi, Z. H.,, I. Hamza,, and M. R. O’Brian. 1999. Heme is an effector molecule for iron dependent degradation of the bacterial iron response regulator (Irr) protein. Proc. Natl. Acad. Sci. USA 96: 13056– 13061.
18.
Qi, Z.,, and M. R. O’Brian. 2002. Interaction between the bacterial iron response regulator and ferrochelatase mediates genetic control of heme biosynthesis. Mol. Cell 9: 155– 162.
19.
Giel,, T. Patschkowski,, C. F. Luther,, J. Ruzicka,, H. Beinert,, and P. J. Kiley. 2001. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. USA 98: 14895– 14900.
20.
Stevens, J. B.,, R. A. Carter,, H. Hussain,, K. C. Carson,, M. J. Dilworth,, and A. W. B. Johnston. 1999. The fhu genes of Rhizobium leguminosarum, specifying siderophore uptake proteins: fhuDCB are adjacent to a pseudogene version of fhuA. Microbiology 145: 593– 601.
21.
Todd, J. D.,, M. Wexler,, G. Sawers,, K. H. Yeoman,, P. S. Poole,, and A. W. B. Johnston. 2002. RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum. Microbiology 148: 4059– 4071.
22.
Visca, P.,, L. Leoni,, M. J. Wilson,, and I. L. Lamont. 2002. Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol. Microbiol. 45: 1177– 1190.
23.
Wexler, M.,, J. D. Todd,, O. Kolade,, A. M. Hemmings,, G. Sawers,, and A. W. B. Johnston. 2003. Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum, Microbiology 149: 1357– 1365.
24.
Wexler, M.,, K. H. Yeoman,, J. B. Stevens,, N. G. de Luca,, G. Sawers,, and A. W. B. Johnston. 2001. The Rhizobium leguminosarum tonB gene is required for the uptake of siderophores and haem as sources of iron. Mol. Microbiol. 41: 801– 816.
25.
Yeoman, K. H.,, A. G. May,, N. G. deLuca,, D. B. Stuckey,, and A. W. B. Johnston. 1999. A putative ECF sigma actor gene, rpoI, regulates siderophore production in Rhizobium leguminosarum. Mol. Plant-Microbiol. Interact. 12: 994– 999.
26.
Yeoman K. H.,, S. Mitelheiser,, G. Sawers,, and A. W. B. Johnston. 2003. The ECF sigma factor RpoI of R. leguminosarum initiates transcription of the vbsGSO and vbsADL siderophore biosynthetic genes in vitro. FEMS Microbiol. Lett. 223: 239– 244.
27.
Yeoman, K. H.,, F. Wisniewski-Dye,, C. Timony,, J. B. Stevens,, N. G. deLuca,, J. A. Dowine,, and A. W. B. Johnston. 2000. Analysis of the Rhizobium leguminosarum siderophore-uptake gene fhuA: differential expression in free-living bacteria and nitrogen- fixing bacteroids and distribution of an fhuA pseudogene in different strains. Microbiology 146: 829– 837.
Tables
Mechanisms and Regulation of Iron Uptake in the Rhizobia
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816544.chap30-1,webId=/content/author/10.1128/9781555816544.chap30-1,properties={foaf_givenname=Andrew W. B., foaf_name=Andrew W. B. Johnston, foaf_surname=Johnston, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816544.chap30-aff1]]}]]
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.tab30-1
TABLE 1
Species of rhizobia referred to in this chapter
10.1128/9781555816544/tab30-1_thmb.gif
10.1128/9781555816544/tab30-1.gif
TABLE 1
Species of rhizobia referred to in this chapter
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.tab30-2
TABLE 2
Proposed functions of individual vbs genes in the VB biosynthetic gene cluster of R. leguminosarum
10.1128/9781555816544/tab30-2_thmb.gif
10.1128/9781555816544/tab30-2.gif
TABLE 2
Proposed functions of individual vbs genes in the VB biosynthetic gene cluster of R. leguminosarum
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30
/content/10.1128/9781555816544.chap30.tab30-3
TABLE 3
Similarities among the Fbp-like proteins of rhizobia and selected homologues in other taxa.
10.1128/9781555816544/tab30-3_thmb.gif
10.1128/9781555816544/tab30-3.gif
TABLE 3
Similarities among the Fbp-like proteins of rhizobia and selected homologues in other taxa.
Citation:
Johnston A.
2004.
Mechanisms and Regulation of Iron Uptake in the Rhizobia,
p 469-488.
In
Crosa J, Mey A, Payne S,
Iron Transport in Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555816544.ch30