Enzymatic Detoxification of Cyanide: Clues from Pseudomonas aeruginosa RhodaneseCipollone R.a · Ascenzi P.a, b · Tomao P.c · Imperi F.a · Visca P.a, b
aDipartimento di Biologia, Università ‘Roma Tre’; bIstituto Nazionale per le Malattie Infettive IRCCS ‘Lazzaro Spallanzani’, Roma, and cDipartimento di Medicina del Lavoro, Istituto Superiore per la Prevenzione e la Sicurezza sul Lavoro, Monteporzio Catone (Roma), Italy
Do you have an account?
- Rent for 48h to view
- Buy Cloud Access for unlimited viewing via different devices
- Synchronizing in the ReadCube Cloud
- Printing and saving restrictions apply
Rental: USD 8.50
Cloud: USD 20.00
Cyanide is a dreaded chemical because of its toxic properties. Although cyanide acts as a general metabolic inhibitor, it is synthesized, excreted and metabolized by hundreds of organisms, including bacteria, algae, fungi, plants, and insects, as a mean to avoid predation or competition. Several cyanide compounds are also produced by industrial activities, resulting in serious environmental pollution. Bioremediation has been exploited as a possible alternative to chemical detoxification of cyanide compounds, and various microbial systems allowing cyanide degradation have been described. Enzymatic pathways involving hydrolytic, oxidative, reductive, and substitution/transfer reactions are implicated in detoxification of cyanide by bacteria and fungi. Amongst enzymes involved in transfer reactions, rhodanese catalyzes sulfane sulfur transfer from thiosulfate to cyanide, leading to the formation of the less toxic thiocyanate. Mitochondrial rhodanese has been associated with protection of aerobic respiration from cyanide poisoning. Here, the biochemical and physiological properties of microbial sulfurtransferases are reviewed in the light of the importance of rhodanese in cyanide detoxification by the cyanogenic bacterium Pseudomonas aeruginosa. Critical issues limiting the application of a rhodanese-based cellular system to cyanide bioremediation are also discussed.
© 2008 S. Karger AG, Basel
- Aird BA, Heinrikson RL, Westley J: Isolation and characterization of a prokaryotic sulfurtransferase. J Biol Chem 1987;262:17327–17335.
- Aminlari M, Li A, Kunanithy V, Scaman CH: Rhodanese distribution in porcine (Sus scrofa) tissues. Comp Biochem Physiol 2002;132:309–313.
- Aminlari M, Shahbazi M: Rhodanese (thiosulfate:cyanide sulfurtransferase) distribution in the digestive tract of chickens. Poult Sci 1994;73:1465–1469.
- Akcil A: Destruction of cyanide in gold mill effluents: biological versus chemical treatments. Biotechnol Adv 2003;21:501–511.
Akcil A, Mudder T: Microbial destruction of cyanide wastes in gold mining: process review. BiotechnolLett 2003;25:445–450.
- Askeland RA, Morrison SM: Cyanide production by Pseudomonasfluorescens and Pseudomonasaeruginosa. Appl Environ Microbiol 1983;45:1802–1807.
ATSDR – Agency for Toxic Substances and Disease Registry: Toxicological Profile for Cyanide. Atlanta, US Department of Health and Human Services, 1997.
- Barclay M, Day JC, Thompson IP, Knowles CJ, Bailey MJ: Substrate-regulated cyanide hydratase (chy) gene expression in Fusariumsolani: the potential of a transcription-based assay for monitoring the biotransformation of cyanide complexes. Environ Microbiol 2002;4:183–189.
- Baxter J, Cummings SP: The current and future applications of microorganism in the bioremediation of cyanide contamination. Antonie Van Leeuwenhoek 2006;90:1–17.
- Beasley DM, Glass WI: Cyanide poisoning: pathophysiology and treatment recommendations. Occup Med (Lond) 1998;48:427–431.
- Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE: The Protein Data Bank. Nucl Acids Res 2000;28:235–242.
- Blumer C, Haas D: Mechanism, regulation, and ecological role of bacterial cyanide biosynthesis. Arch Microbiol 2000;173:170–177.
- Bordo D, Bork P: The rhodanese/Cdc25 phosphatase superfamily. Sequence-structure-function relations. EMBO Rep 2002;3:741–746.
- Bordo D, Deriu D, Colnaghi R, Carpen A, Pagani S, Bolognesi M: The crystal structure of a sulfurtransferase from Azotobactervinelandii highlights the evolutionary relationship between the rhodanese and phosphate enzyme families. J Mol Biol 2000;298:691–704.
- Bordo D, Forlani F, Spallarossa A, Colnaghi R, Carpen A, Bolognesi M, Pagani S: A persulfurated cysteine promotes active site reactivity in Azotobactervinelandii rhodanese. Biol Chem 2001;382:1245–1252.
- Castric PA: Hydrogen cyanide, a secondary metabolite of Pseudomonasaeruginosa. Can J Microbiol 1975;21:613–618.
- Castric PA: Glycine metabolism by Pseudomonasaeruginosa: hydrogen cyanide biosynthesis. J Bacteriol 1977;130:826–831.
- Cipollone R, Ascenzi P, Frangipani E, Visca P: Cyanide detoxification by recombinant bacterial rhodanese. Chemosphere 2006;63:942–949.
- Cipollone R, Ascenzi P, Visca P: Common themes and variations in the rhodanese superfamily. IUBMB Life 2007a;59:51–59.
- Cipollone R, Bigotti MG, Frangipani E, Ascenzi P, Visca P: Characterization of a rhodanese from the cyanogenic bacterium Pseudomonasaeruginosa. Biochem Biophys Res Comm 2004;325:85–90.
- Cipollone R, Frangipani E, Tiburzi F, Imperi F, Ascenzi P, Visca P: Involvement of Pseudomonasaeruginosa rhodanese in protection from cyanide toxicity. Appl Environ Microbiol 2007b;73:390–398.
- Cooper M, Tavankar GR, Williams HD: Regulation of expression of the cyanide-insensitive terminal oxidase in Pseudomonasaeruginosa. Microbiology 2003;149:1275–1284.
- Cunningham L, Pitt M, Williams HD: The cioAB genes from Pseudomonasaeruginosa code for a novel cyanide-insensitive terminal oxidase related to the cytochrome bd quinolon oxidases. Mol Microbiol 1997;24:579–591.
- Cunningham L, Williams HD: Isolation and characterization of mutants defective in the cyanide-insensitive respiratory pathway of Pseudomonasaeruginosa. J Bacteriol 1995;177:432–438.
- Donadio S, Shafiee A, Hutchinson CR: Disruption of a rhodaneselike gene results in cysteine auxotrophy in Saccharopolysporaerythraea. J Bacteriol 1990;172:350–360.
- Dumestre A, Chone T, Portal J, Gerard M, Berthelin J: Cyanide degradation under alkaline conditions by a strain of Fusariumsolani isolated from contaminated soils. Appl Environ Microbiol 1997;63:2729–2734.
- Ebbs S: Biological degradation of cyanide compounds. Curr Opin Biotechnol 2004;15:231–236.
- Ezzi MI, Pascual JA, Gould BJ, Lynch JM: Characterization of the rhodanese enzyme in Trichoderma spp. Enz Microb Technol 2003;32:629–634.
- Fallon RD, Cooper DA, Speece R, Henson M: Anaerobic biodegradation of cyanide under methanogenic conditions. Appl Environ Microbiol 1991;57:1656–1662.
- Felce J, Saier MH Jr: Carbonic anhydrases fused to anion transporters of the SulP family: evidence for a novel type of bicarbonate transporter. J Mol Microbiol Biotechnol 2004;8:169–176.
- Fernández RF, Kunz DA: Bacterial cyanide oxygenase is a suite of enzymes catalyzing the scavenging and adventitious utilization of cyanide as a nitrogenous growth substrate. J Bacteriol 2005;187:6396–6402.
- Fonong T: Enzyme method for the spectrophotometric determination of micro-amounts of cyanide. Analyst 1987;112:1033–1035.
- Forlani F, Cereda A, Freuer A, Nimtz M, Leimkuhler S, Pagani S: The cysteine-desulfurase IscS promotes the production of the rhodanese RhdA in the persulfurated form. FEBS Lett 2005;579:6786–6790.
- Fry WE, Millar RL: Cyanide degradation by an enzyme from Stemphyliumloti. Arch Biochem Biophys 1972;151:468–474.
- Fukumori Y, Hoshiko K, Yamanaka T: Purification and some properties of thiosulphate-cleaving enzyme from Thiobacillus novellus. FEMS Microbiol Lett 1989;65:159–164.
- Gallagher LA, Manoil C: Pseudomonasaeruginosa PAO1 kills Caenorhabditiselegans by cyanide poisoning. J Bacteriol 2001;183:6207–6214.
- Garcia-Horsman JA, Barquera B, Rumbley J, Ma J, Gennis RB: The superfamily of heme-copper respiratory oxidases. J Bacteriol 1994;176:5587–5600.
- Gliubich F, Gazerro M, Zanotti G, Delbono S, Bombieri G, Berni R: Active site structural features for chemically modified forms of rhodanese. J Biol Chem 1996;271:21054–21061.
- Goldfarb WB, Margraf H: Cyanide production by Pseudomonasaeruginosa. Ann Surg 1967;165:104–110.
- Haas D, Dèfago G: Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 2005;3:307–319.
- Han S, Tang R, Anderson LK, Woerner TE, Pei ZM: A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature 2003;425:196–200.
- Harris R, Knowles CJ: Isolation and growth of a Pseudomonas species that utilizes cyanide as a source of nitrogen. J Gen Microbiol 1983;129:1005–1011.
- Ikebukuro K, Shimomura M, Onuma N, Watanabe A, Nomura Y, Nakanishi K, Arikawa Y, Karube I: A novel biosensor system for cyanide based on a chemiluminescence reaction. Anal Chim Acta 1996;329:111–116.
- Ingvorsen K, Hojer-Pedersen B, Godtfredsen SE: Novel cyanide-hydrolysing enzyme from Alcaligenesxylosoxidans subsp. denitrificans. Appl Environ Microbiol 1991;57:1783–1789.
- Knowles CJ: Microorganisms and cyanide. Bacteriol Rev 1976;40:652–680.
- Knowles CJ: Cyanide utilization and degradation by microorganisms. Ciba Found Symp 1988;140:3–15.
- Knowles CJ, Bunch AW: Microbial cyanide metabolism. Adv Microb Physiol 1986;27:73–111.
- Kremer RJ, Souissi T: Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr Microbiol 2001;43:182–186.
- Kunz DA, Wang CS, Chen JL: Alternative routes of enzymic cyanide metabolism in Pseudomonasfluorescens NCIMB 11764. Microbiology 1994;140:1705–1712.
- Laville J, Blumer C, Von Schroetter C, Gaia V, Defago G, Keel C, Haas D: Characterization of the hcnABC gene cluster encoding hydrogen cyanide synthase and anaerobic regulation by ANR in the strictly aerobic biocontrol agent Pseudomonasfluorescens CHA0. J Bacteriol 1998;180:3187–3196.
- Lorck H: Production of hydrocyanic acid by bacteria. Physiol Plant 1948;1:142–146.
Margulis L: Symbiosis in Cell Evolution, ed 2. New York, Freeman, 1993.
- Mattiasson B, Mosbach K: Application of cyanide-metabolizing enzymes to environmental control; enzyme thermistor assay of cyanide using immobilized rhodanese and injectase. Biotechnol Bioeng 1977;19:1643–1651.
- Matthies A, Nimtz M, Leimkuhler S: Molybdenum cofactor biosynthesis in humans: identification of a persulfide group in the rhodanese-like domain of MOCS3 by mass spectrometry. Biochemistry 2005;44:7912–7920.
- Mueller EG, Palenchar PM, Buck CJ: The role of the cysteine residues of ThiI in the generation of 4-thiouridine in tRNA. J Biol Chem 2001;276:33588–33595.
- Nagahara N, Okazaki T, Nishino T: Cytosolic mercaptopyruvate sulfurtransferase is evolutionarily related to mitochondrial rhodanese. J Biol Chem 1995;270:16230–16235.
Oi S: Purification and some properties of Trametes sanguinea rhodanese Agric Biol Chem 1973;37:629–635.
- O’Reilly C, Turner PD: The nitrilase family of CN hydrolising enzymes – a comparative study. J Appl Microbiol 2003;95:1161–1174.
- Pagani S, Sessa G, Sessa F, Colnaghi R: Properties of Azotobactervinelandii rhodanese. Biochem Mol Biol Int 1993;29:595–604.
Paixao MA, Tavares CR, Bergamasco R, Bonifacio AL, Costa RT: Anaerobic digestion from residue of industrial cassava industrialization with acidogenic and methanogenic physical separation phases. Appl Biochem Biotechnol 2000;84–86:809–819.
- Palenchar PM, Buck CJ, Cheng H, Larson TJ, Mueller EG: Evidence that ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate. J Biol Chem 2000;275:8283–8286.
- Papezovà K, Glatz Z: Determination of cyanide in microliter samples by capillary electrophoresis and in capillary enzymatic reaction with rhodanese. J Chromatogr [A] 2006;1120:268–272.
Pessi G, Haas D: Cyanogenesis; in Ramos JL (ed): Pseudomonas: Biosynthesis of Macromolecules and Molecular Metabolism, Dordrecht, Kluwer Academic Publishers, 2004, vol III, pp 671–687.
- Petrozzi S, Dunn IJ: Biological cyanide degradation in aerobic fluized bed reactors: treatment of almond seed wastewater. Bioprocess Eng 1994;11:29–38.
- Ploegman JH, Drent G, Kalk KH, Hol WGJ, Hienrikson RL, Keim P, Wenig L, Russell J: The covalent and tertiary structure of bovine liver rhodanese. Nature 1978;273:124–129.
- Poole RK, Cook GM: Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv Microb Physiol 2000;43:165–224.
- Ray WK, Zeng G, Potters MB, Mansuri AM, Larson TJ: Characterization of a 12-kilodalton rhodanse encoded by glpE of Escherichiacoli and its interaction with thioredoxin. J Bacteriol 2000;182:2277–2284.
- Raybuck SA: Microbes and microbial enzymes for cyanide degradation. Biodegradation 1992;3:3–18.
- Reissmann S, Hochleitner E, Wang H, Paschos A, Lottspeich F, Glass RS, Bock A: Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands. Science 2003;299:1067–1070.
- Ryan RW, Gourlie MP, Tilton RC: Release of rhodanese from Pseudomonasaeruginosa by cold shock and its localization within the cell. Can J Microbiol 1979;25:340–351.
- Ryan RW, Tilton RC: The isolation of rhodanese from Pseudomonasaeruginosa by affinity chromatography. J Gen Microbiol 1977;103:197–199.
Seigler DS: Cyanogenic glycosides and lipids: structural types and distribution; in Vannesland B, Conn EE, Knowles CJ, Westley J, Wissing F (eds): Cyanide in Biology. London, Academic Press, 1981, pp 133–143.
- Silver M, Kelly DP: Rhodanese from Thiobacillus A2: catalysis of reactions of thiosulphate with dihydrolipoate and dihydrolipoamide. J Gen Microbiol 1976;97:277–284.
- Sirko A, Zatyka M, Sadowy E, Hulanicka D: Sulfate and thiosulfate transport in Escherichiacoli K-12: evidence for a functional overlapping of sulfate- and thiosulafate-binding proteins. J Bacteriol 1995;177:4134–4136.
Solomonson LP: Cyanide as a metabolic inhibitor; in Vannesland B, Conn EE, Knowles CJ, Westley J, Wissing F (eds): Cyanide in Biology. London, Academic Press, 1981, pp 11–28.
- Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, Garber RL, Goltry L, Tolentino E, Westbrock-Wadman S, Yuan Y, Brody LL, Coulter SN, Folger KR, Kas A, Larbig K, Lim R, Smith K, Spencer D, Wong GK, Wu Z, Paulsen IT, Reizer J, Saier MH, Hancock RE, Lory S, Olson MV: Complete genome sequence of Pseudomonasaeruginosa PA01, an opportunistic pathogen. Nature 2000;406:959–964.
- Sylvester M, Sander C: Immunohistochemical localization of rhodanese. Histochem J 1990;22:197–200.
- Turkowsky A, Blotevogel KH, Fischer U: Properties of a soluble thiosulfate sulfur transferase (rhodanese) of the marine methanogen Methanosarcina frisia. FEMS Microbiol Lett 1991;81:251–256.
- van Buuren KJ, Nicholis P, van Gelder BF: Biochemical and biophysical studies on cytochrome aa3. VI. Reaction of cyanide with oxidized and reduced enzyme. Biochim Biophys Acta 1972;256:258–276.
- Vetter J: Plant cyanogenic glycosides. Toxicon 2000;38:11–36.
- Voisard C, Keel C, Haas D, Dèfago G: Cyanide production by Pseudomonasfluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 1989;8:351–358.
- Wang SF, Volini M: The interdependence of substrate and protein transformations in rhodanese catalysis. I. Enzyme interactions with substrate, product, and inhibitor anions. J Biol Chem 1973;248:7376–7385.
Westley J: Rhodanese. Adv Enzimol 1973;39:327–368.
Westley J: Depletion of the sulphane pool: toxicological implications; in Damiani LA (ed): Sulphur-Containing Drugs and Related Organic Compounds. New York, Wiley, 1989, vol 2B, pp 87–99.
- Westley J, Adler H, Westley L, Nishida C: The sulfurtransferases. Fundam Appl Toxicol 1983;3:337–382.
- White JM, Jones DD, Huang D, Gauthier JJ: Conversion of cyanide to formate and ammonia by a pseudomonad from industrial wastewater. J Ind Microbiol 1988;3:263–272.
- Wild SR, Rudd T, Neller A: Fate and effects of cyanide during wastewater treatment processes. Sci Total Environ 1994;156:93–107.
- Wissing F: Cyanide formation from oxidation of glycine of Pseudomonas species. J Bacteriol 1974;117:1289–1294.
- Yamasaki M, Matsushita Y, Namura M, Nyunoya H, Katayama Y: Genetic and immunochemical characterization of thiocyanate-degrading bacteria in lake water. Appl Environ Microbiol 2002;68:942–946.
Zhou X, Xu S, Liu L, Chen J: Degradation of cyanide by Trichoderma mutants constructed by restriction enzyme mediated integration (REMI). Bioresour Technol 2006;doi:10. 1016/j.biortech.2006.09.047.
- Zlosnik JEA, Reza G, Bundy JG, Mossialos D, O’Toole R, Williams HD: Investigation of the physiological relationship between cyanide-insensitive oxidase and cyanide production in Pseudomonas aeruginosa. Microbiology 2006;152:1407–1415.
Article / Publication Details
Copyright / Drug Dosage / DisclaimerCopyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.