Abstract
Siderophores are low-molecular weight ligands secreted by bacteria as a survival strategy in Fe(III)-lacking environments. They bind not only Fe(III), but Co(II), Zn(II), Mn(II), Ni(II), Ga(III) as a detoxification alternative. The synthesis, purification and characterization of siderophores produced by Pseudomonas veronii 2E were evaluated to be applied in future environmental technologies. Optimal production was obtained in Fe(III)-free M9-succinate at 25 °C, 40 h and pH 6.9. Siderophores were chemically characterized as hydroxamate and catechol mixed-type. Spectroscopic analysis indicated their belonging to the pyoverdine family, behaving as ligand to Cd(II), Zn(II), Cu(II), Ni(II) and Cr(III), which promoted siderophoregenesis during growth. Siderophore-Cd(II) complexation was studied by electrochemical monitored titration revealing one family of moderate-strength binding sites. Mass spectral analysis evidenced the secretion of a variety of molecules (molecular mass ca.1200 u). Non pathogenic Pseudomonas veronii 2E siderophores represent a safe alternative for the concrete application of environmental technologies and clinical procedures.
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References
Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications: minireview. Microb Biotechnol 7:196–208. https://doi.org/10.1111/1751-7915.12117
Albrecht-Gary A-M, Rochel SN, Ocaktan AZ, Abdallah MA (1994) Bacterial iron transport: coordination properties of pyoverdine PaA, a peptidic siderophore of Pseudomonas aeruginosa. Inorg Chem 33:6391–6402. https://doi.org/10.1021/ic00104a059
Alessandrello M, Vullo DL (2016) Economical fermentation media for the production of a whole cell catalyst for the treatment of Cr(VI)-containing wastewaters. Rev Argent Microbiol 48:245–251
Arnow LE (1973) Colorimetric determination of the components of 3,4-dihydroxyphenylalanine-tyrosine mixtures. J Biol Chem 118:531–537
Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102:11076–11081. https://doi.org/10.1073/pnas.0504266102
Barnum DW (1977) Spectrophotometric determination of catechol, epinephrine, DOPA, dopamine and other aromatic vic-diols. Anal Chim Acta 89:157–166. https://doi.org/10.1016/S0003-2670(01)83081-6
Barrero JM, Moreno-Bondi MC, Pérez-Conde MC, Cámara C (1993) A biosensor for ferric ion. Talanta 40:1619–1623
Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15:325–339
Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ (2009a) New insights into the metals specificity of the Pesudomonas aeruginosa pyoverdine-iron uptake pathway. Environ Microbiol 11:1079–1091. https://doi.org/10.1111/j.1462-2920.2008.01838.x
Braud A, Jézéquel K, Bazot S, Lebeau T (2009b) Enhanced phytoextraction of an agricultural Cr-Hg- and Pb-contaminated soil by bioaugmentation with siderophore producing bacteria. Chemosphere 74:280–286. https://doi.org/10.1016/j.chemosphere.2008.09.013
Braud A, Geoffroy V, Hoegy F, Mislin GL, Schalk IJ (2010) Presence of the siderophores pyoverdine and pyochelin in the extracellular medium reduces toxic metal accumulation in Pseudomonas aeruginosa and increases bacterial metal tolerance. Environ Microbiol Rep 2:419–425. https://doi.org/10.1111/j.1758-2229.2009.00126.x
Braun V, Pramanik A, Gwinner T, Köberle M, Bohn E (2009) Sideromycins: tools and antibiotics. Biometals 22:3–13. https://doi.org/10.1007/s10534-008-9199-7
Budzikiewiez H (1993) Secondary metabolites from fluorescent pseudomonads. FEMS Microbiol Rev 10:209–228
Butaitė E, Kramer J, Wyder S, Kümmerli R (2018) Environmental determinants of pyoverdine production, exploitation and competition in natural Pseudomonas communities. Environ Microbiol. https://doi.org/10.1111/1462-2920.14355
Cézard C, Farvacques N, Sonnet P (2015) Chemistry and biology of pyoverdines, Pseudomonas primary siderophores. Curr Med Chem 22:165–186
Chen Y, Jurkevitch E, Bar-Ness E, Hadar Y (1994) Stability constants of pseudobactin complexes with transition metals. Soil Sci Soc Am J 58:390–396
Colquhoun DJ, Sørum H (2001) Temperature dependent siderophore production in Vibrio salmonicida. Microb Pathog 31:213–219. https://doi.org/10.1006/mpat.2001.0464
Cornelis P, Matthijs S (2007) Pseudomonas siderophores and their biological significance. In: Varma A, Chincholkar SB (eds) Microbial siderophore. Springer, Berlin, pp 121–133
Cornu JY, Elhabiri M, Ferret C, Geoffroy VA, Jezequel K, Leva Y, Lollier M, Schalk IJ, Lebeau T (2014) Contrasting effects of pyoverdine on the phytoextraction of Cu and Cd in a calcareous soil. Chemosphere 103:212–219. https://doi.org/10.1016/j.chemosphere.2013.11.070
Cox CD, Graham R (1979) Isolation of an iron-binding compound from Pseudomonas aeruginosa. J Bacteriol 37:1357–1364
Crowley D (2006) Microbial siderophores in plant rhizosphere. In: Barton L, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 169–189
Csáky TZ (1948) On the estimation of bound hydroxylamine in biological materials. Acta Chem Scand 2:450–454. https://doi.org/10.3891/acta.chem.scand.025-0450
Daniel M, Barrionuevo M, Doyle S, Vullo DL (2016) Kinetics of Pseudomonas veronii 2E biofilm development under. Biochem Eng J 105:150–158. https://doi.org/10.1016/j.bej.2015.09.001
Danil de Namor AF, El Gamouz A, Frangie S, Martinez V, Valiente L, Webb OA (2012) Turning the volume down on heavy metals using tuned diatomite. A review of diatomite and modified diatomite for the extraction of heavy metals from water. J Hazard Mater 241–242:14–31
Daveu C, Servy C, Dendane M, Marin P, Ducrocq C (1997) Oxidation and nitration of catecholamines by nitrogen oxides derived from nitric oxide. Nitric Oxide Biol Ch 1:234–243. https://doi.org/10.1006/niox.1997.0123
Demange P, Wendenbaum S, Bateman A, Dell A, Meyer JM, Abdallah MA (1987) Bacterial siderophores: structure and physicochemical properties of pyoverdins and related compounds. In: Winkelmann G, van der Helm D, Neilands JB (eds) Iron transport in microbes, plants and animals. VCH, Weinkeim, pp 167–187
Dimkpa C, Merten D, Svatos A, Büchel G, Kothe E (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696. https://doi.org/10.1111/j.1365-2672.2009.04355.x
Duffus JH (2002) “Heavy metals"-A meaningless term? Pure Appl Chem 74:793–807
Edberg F, Kalinowski BE, Holmström SJM, Holm K (2010) Mobilization of metals from uranium mine waste: the role of pyoverdines produced by Pseudomonas fluorescens. Geobiology 8:278–292. https://doi.org/10.1111/j.1472-4669.2010.00241.x
Ferreira ML, Casabuono AC, Stacchiotti ST, Couto AS, Ramirez SA, Vullo DL (2017) Chemical characterization of Pseudomonas veronii 2E soluble exopolymer as Cd(II) ligand for the biotreatment of electroplating wastes. Int Biodeterior Biodegrad 119:605–613. https://doi.org/10.1016/j.ibiod.2016.10.013
Fuchs R, Schäfer M, Geoffroy V, Meyer JM (2001) Siderotyping-a powerful tool for the characterization of pyoverdines. Curr Top Med Chem 1:31–57. https://doi.org/10.2174/1568026013395542
Garavaglia L, Cerdeira SB, Vullo DL (2010) Chromium (VI) biotransformation by beta- and gamma-proteobacteria from natural polluted environments: a combined biological and chemical treatment for industrial wastes. J Hazard Mater 15:104–110. https://doi.org/10.1016/j.jhazmat.2009.09.134
Gillam AH, Lewis AG, Andersen RJ (1981) Quantitative determination of hydroxamic acids. Anal Chem 53:841–844. https://doi.org/10.1021/ac00229a023
Guan LL, Kanoh K, Kamino K (2001) Effect of exogenous siderophores on iron uptake activity of marine bacteria under iron-limited conditions. Appl Environ Microbiol 4:1710–1717. https://doi.org/10.1128/AEM.67.4.1710-1717.2001
Huang Y, Jiang Y, Wang H, Wang J, Shin MC, Byun Y, He H, Liang Y, Yang VC (2013) Curb challenges of the “Trojan Horse” approach: smart strategies in achieving effective yet safe cell-penetrating peptide-based drug delivery. Adv Drug Deliv Rev 65:1299–1315. https://doi.org/10.1016/j.addr.2012.11.007
Johnstone T, Nolan E (2015) Beyond iron: non-classical biological functions of bacterial siderophores. Dalton Trans 44:6320–6339. https://doi.org/10.1039/C4DT03559C
Kumar B, Dube H (1991) Plant growth-promoting activity of fluorescent Pseudomonas from tomato rhizoplane. Indian J Exp Biol 29:366–370
Lutkenhaus JF (1977) Role of mayor outer membrane protein in Escherichia coli. J Bacteriol 131:631–637
Martell E, Smith R (2010) NIST standard reference database 46. NIST critically selected stability constants of metal complexes. Version 8.0. http://www.nist.gov/srd/nist46.cfm
Masalha J, Kosegarten H, Elmaci O, Mengel K (2000) The central role of microbial activity for iron acquisition in maize and sunflower. Biol Fertil Soils 30:433–439. https://doi.org/10.1007/s003740050
Mehri I, Khessairi A, Turki Y (2012) Effect of dose-response of zinc and manganese on siderophore production. Am J Environ Sci 8:143–151
Méndez N, Ramírez S, Ceretti H, Zalts A, Candal R, Vullo DL (2011) Pseudomonas veronii 2E surface interactions with Zn(II) and Cd(II). Global J Environ Sci Technol 1:3
Merja M, Tiina M-S (1994) Methods for detection of Pseudomonas siderophores. J Microbiol Methods 19:223–234
Meyer JM, Abdallah MA (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. J Gen Microbiol 107:319–328. https://doi.org/10.1099/00221287-107-2-319
Meyer JM, Stintzi A, De Vos D, Cornelis P, Tappe R, Taraz K, Budzikiewicz H (1997) Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143:35–43. https://doi.org/10.1099/00221287-143-1-35
Meyer JM, Geoffroy VA, Baida N, Gardan L, Izard D, Lemanceau P, Achouak W, Palleroni NJ (2002) Siderophore typing, a powerful tool for the identification of fluorescent and nonfluorescent Pseudomonas. Appl Environ Microbiol 68:2745–2753. https://doi.org/10.1128/AEM.68.6.2745-2753.2002
Miethke M, Marahiel M (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 7:413–451. https://doi.org/10.1128/MMBR.00012-07
Mollmann U, Heinisch L, Bauernfeind A, Kohler T, Ankel-Fuchs D (2009) Siderophores as drug delivery agents: application of the “Trojan Horse” strategy. Biometals 22:615–624. https://doi.org/10.1007/s10534-009-9219-2
Nair A, Juwarkar A, Singh S (2007) Production and characterization of siderophores and its applications in arsenic removal from contaminated soil. Water Air Soil Pollut 180:199–212
Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726
Nieboer E, Richardson D (1980) The replacement of the nondescript term heavy metals by a biologically and chemically significant classification of metal ions. Environ Pollut 1:3–26
Paine SM (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol 235:329–344
Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149. https://doi.org/10.1016/j.tibtech.2009.12.002
Ramirez SA, Zalts A, Fernández Morantes C, Torres Sánchez RM, Sosa GL (2017) Adsorción de Zn(II) en diatomitas modificadas con ligandos: estudios en equilibrio para su aplicación en el tratamiento de efluentes. In: Aspromonte S, Boix A, Bosko L, Gomez L (eds) Ambiente y desarrollo sostenible desde una perspectiva multidisciplinaria. Sociedad Argentina de Ciencia y Tecnologia Ambiental, Buenos Aires, pp 483–488
Raymond KN, Dertz EA, Kim SS (2003) Enterobactin: an archetype for microbial iron transport. Proc Natl Acad Sci USA 100:3584–3588. https://doi.org/10.1073/pnas.0630018100
Rioux C, Jordan DC, Rattray JB (1983) Colorimetric determination of catechol siderophores in microbial cultures. Anal Biochem 133:163–169
Ružić I (1996) Trace metal complexation at heterogeneous binding sites in aquatic systems. Mar Chem 53:1–15. https://doi.org/10.1016/0304-4203(96)00008-4
Saha R, Saha N, Donofrio RS, Bestervelt LL (2012) Microbial siderophores: a mini review. J Basic Microbiol 52:1–15. https://doi.org/10.1002/jobm.201100552
Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharjee S, Tribedi P (2016) Microbial siderophores and their potential applications: a review. Environ Sci Pollut Res Int 23:3984–3999. https://doi.org/10.1007/s11356-015-4294-0
Sayyed RZ, Badgujar MD, Sonawane HM, Mhaske MM, Chincholkar SB (2005) Production of microbial iron chelators (siderophores) by fluorescent Pseudomonads. Indian J Biotechnol 4:484–490
Scatchard G (1949) The attractions of proteins for small molecules and ions. Ann NY Acad Sci 51:660–672. https://doi.org/10.1111/j.1749-6632.1949.tb27297.x
Schalk IJ, Hannauer M, Braud A (2011) New role for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854. https://doi.org/10.1111/j.1462-2920.2011.02556.x
Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56
Srideri M, Kumar KG, Mallaiah KV (2008) Production of catechol-type os siderophores by Rhizobium sp. isolated from stem nodules of Sesbania procumbens (Roxb.) W and A. Res J Microbiol 3:282–287. https://doi.org/10.3923/jm.2008.282.287
Sulochana MB, Jayachandra SY, Anil Kumar S, Parameshwar AB, Mohan Reddy K, Dayanand A (2014) Siderophore as a potential plant growth-promoting agent produced by Pseudomonas aeruginosa JAS-25. Appl Biochem Biotechnol 174:297–308. https://doi.org/10.1007/s12010-014-1039-3
Tortora ML, Diaz-Ricci JC, Pedraza RO (2011) Azospirillum brasilense siderophore with antifungal activity against Colletotrichum acutatum. Arch Microbiol 193:275–286. https://doi.org/10.1007/s00203-010-0672-7
Velasquez I, Nunn BL, Ibisanmi E, Goodlett DR, Hunter KA, Sander SG (2011) Detection of hydroxamate siderophores in coastal and Sub-Antartic waters off the South Eastern Coast of New Zeland. Mar Chem 126:97–107. https://doi.org/10.1016/j.marchem.2011.04.003
Visca P, Colotti G, Serino L, Verzili D, Orsi N, Chiancone E (1992) Metal regulation of siderophore synthesis in Pseudomonas aeruginosa and functional effects of siderophore-metal complexes. Appl Environ Microbiol 58:2886–2893
Visca P, Leoni L, Wilson MJ, Lamont IL (2002) Iron transport and regulation, cell signaling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45:1177–1190
Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15:22–30. https://doi.org/10.1016/j.tim.2006.11.004
Vullo DL, Ceretti HM, Daniel MA, Ramirez SA, Zalts A (2008) Cadmium, zinc and copper biosorption mediated by Pseudomonas veronii 2E. Bioresour Technol 99:5574–5581. https://doi.org/10.1016/j.biortech.2007.10.060
Worsham PL, Konisky J (1984) Effect of growth temperature on the acquisition of iron by Salmonella typhimurium and Escherichia coli. J Bacteriol 158:163–168
Ye L, Ballet S, Hildebrand F, Laus G, Guillemyn K, Raes J, Matthijs S, Martins J, Cornelis P (2013) A combinatorial approach to the structure elucidation of pyoverdine siderophore produced by a Pseudomonas putida isolate and the use of pyoverdine as a taxonomic marker for typing P. putida subspecies. Biometals 26:561–575. https://doi.org/10.1007/s10534-013-9653-z
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This work was financially supported by the Universidad Nacional de General Sarmiento, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), PIO CONICET-YPF No. 13320130100204CO, and Agencia Nacional de Promoción Científica y Tecnológica (PICT 2014 No. 0964). The authors are grateful to Miss Leticia Rossi for the English language revision.
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Ferreira, M.L., Ramirez, S.A. & Vullo, D.L. Chemical characterization and ligand behaviour of Pseudomonas veronii 2E siderophores. World J Microbiol Biotechnol 34, 134 (2018). https://doi.org/10.1007/s11274-018-2519-3
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DOI: https://doi.org/10.1007/s11274-018-2519-3