Abstract
Most species of the genus Aeromonas produce the siderophore amonabactin, although two species produce enterobactin, the siderophore of many enteric bacteria. Both siderophores contain 2,3-dihydroxybenzoic acid (2,3-DHB). Siderophore genes (designated aebC, -E, -B and -A, for aeromonad enterobactin biosynthesis) that complemented mutations in the enterobactin genes of the Escherichia coli 2,3-DHB operon, entCEBA(P15), were cloned from an enterobactin-producing isolate of the Aeromonas spp. Mapping of the aeromonad genes suggested a gene order of aebCEBA, identical to that of the E. coli 2,3-DHB operon. Gene probes for the aeromonad aebCE genes and for amoA (the entC-equivalent gene previously cloned from an amonabactin-producing Aeromonas spp.) did not cross-hybridize. Gene probes for the E. coli 2,3-DHB genes entCEBA did not hybridize with Aeromonas spp. DNA. Therefore, in the genus Aeromonas, 2,3-DHB synthesis is encoded by two distinct gene groups; one (amo) is present in the amonabactin-producers, while the other (aeb) occurs in the enterobactin-producers. Each of these systems differs from (but is functionally related to) the E. coli 2,3-DHB operon. These genes may have diverged from an ancestral group of 2,3-DHB genes.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Andrus C, Payne SM. 1983 Siderophores and iron regulated proteins in Vibrio and Aeromonas species. Abstr Annu Meet Am Soc Microbiol D-13, 61.
Angerer A, Klupp B, Braun V. 1992 Iron transport systems of Serratia marcescens. J Bacteriol 174, 1378–1387.
Bachhwat A, Ghosh S. 1987 Iron transport in Azospirillum brasilense: role of the siderophore spirilobactin. J Gen Microbiol 133, 1759–1765.
Barghouthi S, Young R, Olson MOJ, Arceneaux JEL, Clem LW, Byers BR. 1989 Amonabactin, a novel tryptophan- or phenylalanine-containing phenolate siderophore in Aeromonas hydrophila. J Bacteriol 171, 1811–1816.
Barghouthi S, Payne SM, Arceneaux JEL, Byers BR. 1991 Cloning, mutagenesis, and nucleoide sequence of a siderophore biosynthetic gene (amoA) from Aeromonas hydrophila. J Bacteriol 173, 5121–5128.
Brickman TJ, Ozenberger BA, McIntosh MA. 1990 Regulation of divergent transcription from the iron-responsive fepB-entC promoter-operator regions in Escherichia coli. J Mol Biol 212, 669–682.
Bull CT, Loper JE. 1991 Genetic analysis of catechol siderophore production of Erwinia carotovora. Phytopathology 81, 1187.
Byers BR. 1987 Pathogenic iron acquisition. Life Chem Rep 4, 143–159.
Byers BR, Arceneaux JEL. 1993 Siderophore diversity in the genus Aeromonas. Med Microbiol Lett 2, 281–285.
Chakraborty RN, Patel HN, Desai SB. 1990 Isolation and partial characterization of a catechol-type siderophore in Pseudomonas stutzeri RC 7. Curr Microbiol 20, 283–286.
Corbin JL, Bulen WA. 1969 The isolation and identification of 2,3-dihydroxybenzoic acid and 2-N,6-N-di(2,3-dihydroxy-benzoyl)-L-lysine formed by iron-deficient Azotobacter vinelandii. Biochemistry 8, 757–762.
Davis RW, Botstein D, Roth JR. 1980 Advanced Bacterial Genetics, A Manual for Genetic Engineering. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Dyer JR, Heding H, Schaffer CP. 1964 Phenolic metabolite of ‘low iron fermentation’ of Streptomyces griseus. Characterization of 2,3-dihydroxybenzoic acid. J Org Chem 29, 2802–2803.
Echenique JR, Arienti H, Tolmasky ME, et al. 1992 Characterization of a high-affinity iron transport system in Acinetobacter baumannii. J Bacteriol 174, 7670–7679.
Faundez G, Aron L, Cabello FC. 1990 Chromosomal DNA, iron-transport systems, outer membrane proteins, and enterotoxin (heat labile) production in Salmonella typhi strains. J Clin Microbiol 28, 894–897.
Fleming TP, Nahlik MS, Neilands JB, McIntosh MA. 1985 Physical and genetic characterization of cloned enterobactin genomic sequences from Escherichia coli K-12. Gene 34, 47–54.
Franza T, Expert D. 1991 The virulence-associated chrysobactin iron uptake system of Erwinia chrysanthemi 3937 involves an operon encoding transport and biosynthetic functions. J Bacteriol 173, 6874–6881.
Franza T, Enard C, Gijsegem FV, Expert D. 1991 Genetic analysis of the Erwinia chrysanthemi 3937 chrysobactin iron-transport system: characterization of a gene cluster involved in transport and biosynthetic pathways. Mol Microbiol 5, 1319–1329.
Grossman TH, Tuckman M, Ellestad S, Osburne MS. 1993 Isolation and characterization of Bacillus subtilis genes involved in siderophore biosynthesis: relationship between B. subtilis sfp 0 and Escherichia coli entD genes. J Bacteriol 175, 6203–6211.
Griffiths GL, Sigel SP, Payne SM, Neilands JB. 1984 Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem 259, 383–385.
Ito T, Neilands JB. 1958 Products of ‘low-iron fermentation’ with Bacillus subtilis: isolation, characterization and synthesis of 2,3-dihydroxybenzoylglycine. J Am Chem Soc 80, 4645–4647.
Jadhav RS, Desai AJ. 1992 Characterization of siderophore from cowpea Rhizobium (peanut isolate). Curr Microbiol 24, 137–141.
Jalal MA, Hossain MB, van der Helm D, Sanders-Loehr J, Actis LA, Crosa JH. 1989 Structure of anguibactin, a unique plasmid-related bacterial siderophore from the fish pathogen Vibrio anguillarum. J Am Chem Soc 111, 292–296.
Knosp O, von Tigerstrom M, Page WJ. 1984 Siderophore-mediated uptake of iron in Azotobacter vinelandii. J Bacteriol 159, 337–341.
Kobaru S, Tsunakawa M, Hanada M, Konishi M, Tomita K, Kawaguchi H. 1983 Bu-2743E, a leucine aminopeptidase inhibitor produced by Bacillus circulans. J Antibiot 36, 1396–1398.
Korth H. 1970 Über das Vorkommen von 2,3-Dihydroxybenzoesäure und ihrer Amino-säurederivate in Kulturmedien von Klebsiella oxytoca. Arch Mikrobiol 70, 297–302.
Kunze B, Bedorf N, Kohl W, Höfle G, Reichenbach H. 1989 Myxochelin A, a new iron-chelating compound from Angiococcus disciformis (myxobacteriales). J Antibiot 42, 14–17.
Liu J, Duncan K, Walsh CT. 1989 Nucleotide sequence of a cluster of Escherichia coli enterobactin biosynthesis genes: identification of entA and purification of its product 2,3-dihydro-2,3-dihydroxybenzoate dehydrogenase. J Bacteriol 171, 791–798.
Liu J, Quinn N, Berchtold GA, Walsh CT. 1990 Overexpression, purification, and characterization of isochorismate synthase (EntC), the first enzyme involved in the biosynthesis of enterobactin from chorismate. Biochemistry 29, 1417–1425.
Lopez-Goni I, Moriyon I, Neilands JB. 1992 Identification of 2,3-dihydroxybenzoic acid as the Brucella abortus siderophore. J Bacteriol 60, 4496–4503.
Maniatis T, Fritsch EF, Sambrook J. 1982 Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Marmur J. 1961 A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3, 208–218.
Matzanke BF. 1991 Structures, coordination chemistry and functions of microbial iron chelates, In: Winkelmann G, ed., CRC Handbook of Microbiol Iron Chelates. Boca Raton, FL: CRC Press.
Miller JH. 1972 Experiments in Molecular Biology. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
Modi H, Shah KS, Modi VV. 1985 Isolation and characterization of catechol like siderophore from cowpea Rhizobium RA-1. Arch Microbiol 141, 156–158.
Nahlik MS, Fleming TP, McIntosh MA. 1987 Cluster of genes controlling synthesis and activation of 2,3-dihydroxybenzoic acid in production of enterobactin in Escherichia coli. J Bacteriol 169, 4163–4170.
Nahlik MS, Brickman TJ, Ozenberger BA, McIntosh MA. 1989 Nucleotide sequence and transcriptional organization of the Escherichia coli enterobactin biosynthesis cistrons entB and entA. J. Bacteriol 171, 784–790.
O'Brien IG, Gibson F. 1970 The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli. Biochim Biophys Acta 215, 393–402.
Ong SA, Peterson T, Neilands JB. 1979 Agrobactin, a siderophore from Agrobacterium tumefaciens. J Biol Chem 254, 1860–1865.
Ozenberger BA, Brickman TJ, McIntosh MA. 1989 Nucleotide sequence of Escherichia coli isochorismate synthetase gene entC and evolutionary relationship of isochorismate synthetase and other chorismate-utilizing enzymes. J Bacteriol 171, 775–783.
Payne SM, Niesel DW, Peixotto SS, Lawlor KM. 1983 Expression of hydroxamate and phenolate siderophores by Shigella flexneri. J Bacteriol 155, 949–955.
Patel HN, Chakraborty RN, Desai SB. 1988 Isolation and partial characterization of a phenolate siderophore from Rhizobium leguminosarum IARI 102. FEMS Microbiol Lett 56, 131–134.
Page WJ, Von Tigerstrom M. 1988 Aminochelin, a catecholamine siderophore produced by Azotobacter vinelandii. J Gen Microbiol 134, 453–460.
Perry RD, San Clemente CL. 1979 Siderophores synthesis in Klebsiella pneumoniae and Shigella sonnei during iron deficiency. J Bacteriol 140, 1129–1132.
Persmark M, Expert D, Neilands JB. 1989 Isolation, characterization, and synthesis of chrysobactin, a compound with siderophore activity from Erwinia chrysanthemi. J Biol Chem 264, 3187–3189.
Pickett CL, Hayes L, Earhart CF. 1984 Molecular cloning of the Escherichia coli K-12 entACGBE genes. FEMS Microbiol Lett 24, 77–80.
Podschun R, Fischer A, Ullman U. 1992 Siderophore production of Klebsiella species isolated from different sources. Zbl Bakt 276, 481–486.
Pollack JR, Neilands JB. 1970 Enterobactin, an iron transport compound from Salmonella typhimurium. Biochem Biophys Res Commun 38, 989–992.
Ratledge C, Chaudrey MA. 1971 Accumulation of iron-binding phenolic acids by actinomycetales and other organisms related to mycobacteria. J Gen Microbiol 66, 71–78.
Rusnak F, Faraci WS, Walsh CT. 1989 Subcloning, expression, and purification of the enterobactin biosynthetic enzyme 2,3-dihydroxybenzoate-AMP ligase: demonstration of enzyme-bound (2,3-dihydroxybenzoyl)adenylate product. Biochemistry 28, 6827–6835.
Rusnak F, Liu J, Quinn N, Berchtold GA, Walsh CT. 1990 Subcloning of the enterobactin biosynthetic gene entB: expression, purification, characterization, and substrate specificity of isochorismatase. Biochemistry 29, 1425–1435.
Saxena B, Modi M, Modi VV. 1986 Isolation and characterization of siderophores from Azospirillum lipoferum D2. J Gen Microbiol 132, 2219–2224.
Schmitt MP, Payne SM. 1988 Genetics and regulation of enterobactin genes in Shigella flexneri. J Bacteriol 170, 5579–5587.
Schmitt MP, Payne SM. 1991 Genetic analysis of the enterobactin gene cluster in Shigella flexneri. J Bacteriol 173, 816–825.
Skorupska A, Choma A, Derylo H, Lorkiewicz Z. 1988 Siderophore containing 2,3-dihydroxybenzoic acid and threonine formed by Rhizobium trifolii. Acta Biochim Pol 35, 119–130.
Simon R, Priefer V, Puhler A. 1983 A broad host range mobilization system for in vivo genetic engineering and transposon mutagenesis in gram negative bacteria. Biotechnology 1, 784–791.
Smith AW, Freeman S, Minnet WG, Lambert PA. 1990 Characterization of a siderophore from Acinetobacter calcoaceticus. FEMS Microbiol Lett 70, 29–32.
Staab JF, Earhart CF. 1990 EntG activity of Escherichia coli enterobactin synthetase. J Bacteriol 172, 6403–6410.
Stoebner JA, Payne SM. 1988 Cloning and characterization of the vibriobactin genes of Vibrio cholerae. Abstr Annu Meet Am Soc Microbiol D-182, 101.
Tait GT. 1975 The identification and biosynthesis of siderochromes formed by Micrococcus denitrificans. Biochem J 146, 191–204.
Taraz K, Ehlert G, Geisen K, Budzikiewicz H. 1990 Protochelin, ein Catecholat-Siderophor aus einem Bakterium (DMS Nr. 5746). Z Naturforsch 45, 1327–1332.
Tarkkanen A-M, Allen BL, Williams PH, et al. 1992 Fimbriation, capsulation, and iron-scavenging systems of Klebsiella strains associated with human urinary tract infection. Infect Immun 60, 1187–1192.
Yamamoto S, Okujo N, Fujita Y, Saito M, Yoshida T, Shinoda S. 1993 Structures of two polyamine-containing caatecholate siderophores from Vibrio fluvialis. J Biochem 113, 538–544.
Zywno SR, Arceneaux JEL, Altwegg M, Byers BR. 1992 Siderophore production and DNA hybridization groups of Aeromonas spp. J Clin Microbiol 30, 619–622.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Massad, G., Arceneaux, J.E.L. & Byers, B.R. Diversity of siderophore genes encoding biosynthesis of 2,3-dihydroxybenzoic acid in Aeromonas spp.. Biometals 7, 227–236 (1994). https://doi.org/10.1007/BF00149553
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00149553