Abstract
Cyanide is one of the most poisonous substances in the environment, which may have originated from natural and anthropogenic sources. There are many enzymes produced by microorganisms which can degrade and utilize cyanide. The major byproducts of cyanide degradation are alanine, glutamic acid, alpha-amino-butyric acid, beta-cyanoalanine, pterin etc. These products have many pharmaceutical and medicinal applications. For the degradation of cyanide, microbes produce necessary cofactors which catalyze the degradation pathways. Pterin is one of the cofactors for cyanide degradation. There are many pathways involved for the degradation of cyanide, cyanate, and thiocyanate. Some of the microorganisms possess resistance to cyanide, since they have developed adaptive alternative pathways for the production of ATP by utilization of cyanide as carbon and nitrogen sources. In this review, we summarized different enzymes, their mechanisms, and corresponding pathways for the degradation of cyanide and production of pterins during cyanide degradation. We aim to enlighten different types of pterin, its classification, and biological significance through this literature review.
Similar content being viewed by others
References
Knowles CJ, Bunch AW (1986) Microbial cyanide metabolism. Adv Microb Physiol 27:73–111
Mudder T, Chadwick J (2001) The cyanide guide special issue of mining environmental management. Min J Ltd 9:45 (ISSN 0969–4218)
Zajtchuk R, Bellamy (1997) Medical aspects of chemical and biologic warfare, textbook of military medicine. Borden Institute, Washington
Gurbuz F, Ciftci H, Akcil A, Karahan AG (2004) Microbial detoxification of cyanide solutions: a new biotechnological approach using algae. Hydrometallurgy 72:167–176. https://doi.org/10.1016/j.hydromet.2003.10.004
Fairbrother L, Shapter J, Brugger J, Southam G, Pring A, Reith F (2009) Effect of the cyanide-producing bacterium Chromobacterium violaceum on ultraflat Au surfaces. Chem Geol 265:313–320. https://doi.org/10.1016/j.chemgeo.2009.04.010
Gurbuza F, Ciftci H, Akcilb A (2009) Biodegradation of cyanide containing effluents by Scenedesmus obliquus. J Hazard Mater 162:74–79. https://doi.org/10.1016/j.jhazmat.2008.05.008
Barclay M, Hart A, Knowles CJ, Meeussen JCL, Tett VA (1998) Biodegradation of metal cyanides by mixed and pure cultures of fungi. Enzyme Microb Technol 22:223–231
Barclay M, Tett VA, Knowles CJ (1998) Metabolism and enzymology of cyanide/metallocyanide biodegradation by Fusarium solani under neutral and acidic conditions. Enzyme Microb Technol 23:321–330
Ezzi MI, Lynch JM (2005) Biodegradation of cyanide by Trichoderma spp. and Fusarium spp. Enzyme Microb Technol 36:849–854
Huertas MJ, Saez LP, Roldan MD, Luque-Almagro VM, Martı´nez-Luque M, Blasco R, Castillo F, Moreno-Vivian C, Garcı´a-Garcı´a I (2010) Alkaline cyanide degradation by Pseudomonas pseudoalcaligenes CECT5344 in a batch reactor. Influence of pH. J Hazard Mater 179:72–78. https://doi.org/10.1016/j.jhazmat.2010.02.059
Kunz DA, Nagappan O, Silva-Avalos J, Delong GT (1992) Utilization of cyanide as a nitrogenous substrate by Pseudomonas fluorescens NCIMB 11764: evidence for multiple pathways of metabolic conversion. Appl Environ Microbiol 58:2022–2029
Ozel YK, Gedikli S, Aytar P, Unal A, Yamac M, Cabuk A, Kolankaya N (2010) New fungal biomasses for cyanide biodegradation. J Biosci Bioeng 110(4):431–435. https://doi.org/10.1016/j.jbiosc.2010.04.011
Park D, Lee DS, Kim YM (2008) Bioaugmentation of cyanide-degrading microorganisms in a full-scale cokes wastewater treatment facility. Bioresour Technol 99:2092–2096. https://doi.org/10.1016/j.biortech.2007.03.027
Luque-Almagro VM, Huertas MJ, Martı´nez-Luque M, Moreno-Vivian C, Roldan D, Garcı´a Gil LJ, Castillo F, Blasco R (2005) Bacterial degradation of cyanide and its metal complexes under alkaline conditions. Appl Environ Microbiol 71:940–947. https://doi.org/10.1128/AEM.71.2.940-947.2005
Tiong B, Bahari ZM, Lee NS, Jaafar J, Ibrahim Z, Shahir S (2015) Cyanide degradation by pseudomonas pseudoalcaligenes strain W2 isolated from mining effluent. Sains Malays 44(2):233–238
Moradkhani M, Yaghmaei S, Nejad ZG (2018) Biodegradation of cyanide under alkaline conditions by a strain of Pseudomonas putida isolated from gold mine soil and optimization of process variables through response surface methodology (RSM). Period Polytech Chem Eng 62:265–273
Dorr PK, Knowles CJ (1989) Cyanide oxygenase and cyanase activities of Pseudomonas fluorescens NCIMB 11764. FEMS Microbiol Lett 60:289–294. https://doi.org/10.1111/j.1574-6968.1989.tb03488.x
Harris R, Knowles CJ (1983) Isolation and growth of pseudomonas species that utilizes cyanide as source of nitrogen. J Gen Microbiol 129:1005–1011
Chatpawala KD, Babu GRV, Vijaya OK, Kumar KP, Wolfram JH (1998) Biodegradation of cyanides, cyanates and thiocyanates to ammonia and carbon dioxide by immobilized cells of Pseudomonas putida. J Ind Microbiol Biotechnol 20:28–33. https://doi.org/10.1038/sj.jim.2900469
Avcioglu NH, Bilkay IS (2016) Biological treatment of cyanide by using Klebsiella pneumonia species. Food technol Biotechnol 54:450–454. https://doi.org/10.17113/ftb.54.04.16.45188
Chaudhari AU, Kodam KM (2010) Biodegradation of thiocyanate using co-culture of Klebsiella pneumoniae and Ralstonia sp. Appl Microbiol Biotechnol 85:1167–1174. https://doi.org/10.1007/s00253-009-2299-7
Kao CM, Liu JK, Lou HR, Lin CS, Chen SC (2003) Biotransformation of cyanide to methane and ammonia by Klebsiella oxytoca. Chemosphere 50:1055–1061
Adjei MD, Ohta Y (2000) Factors affecting the biodegradation of cyanide by Burkholderia cepacia C-3. J Biosci Bioeng 89:274–277. https://doi.org/10.1016/S1389-1723(00)88833-7
Potivichayanon S, Kitleartpornpairoat R (2010) Biodegradation of cyanide by a novel cyanide-degrading bacterium. World Acad Sci Eng Technol 42:1362–1365
Macadam AM, Knowles CJ (1984) Purification and properties of β-cyano alanine synthase from the cyanide-producing bacterium. Chromobacterium Violaceum Biochim Biophys Acta 786:123–132. https://doi.org/10.1016/0167-4838(84)90081-5
Fry WE, Millar RL (1972) Cyanide degradation by an enzyme from Stemphylium loti. Arch Biochem Biophys 151:468–474
Luque-Almagro VM, Moreno-Vivián C, Roldán MD (2016) Biodegradation of cyanide wastes from mining and jewellery industries. Curr Opin Biotechnol 38:9–13. https://doi.org/10.1016/j.copbio.2015.12.004
Murugesan T, Durairaj N, Ramasamy M, Jayaraman K, Palaniswamy M, Jayaraman A (2017) Analeptic agent from microbes upon cyanide degradation. Appl Microbiol Biotechnol 102(4):1557–1565
Adjei MD, Ohta Y (1999) Isolation and characterization of a cyanide utilizing Burkholderia cepacia strain. World J Microbiol Biotechnol 15:699–704
Sexton AC, Howlett BJ (2000) Charcterisation of cyanide hydratase gene in the phytopathogeneic fungus leptosphaeria maculans. Mol Gen Genet 263:463–470
Yanase H, Sakamoto A, Okamoto K, Kita K, Sato Y (2000) Degradation of the metal cyano complex tetracyanonickelate (II) by Fusarium oxysporum N-10. Appl Microbiol Biotechnol 53:328–334. https://doi.org/10.1007/s002530050029
Baxter J, Cummings SP (2006) The current and future applications of microoorganism in the bioremediation of cyanide contamination. Antonie Van Leeuwenhoek 90:1–17. https://doi.org/10.1007/s10482-006-9057-y
Urbanska A, Leszczynshi B, Matok H, Dixon AFG (2002) Cyanide detoxifying enzymes of bird cherry oat aphid. Electron J Pol Agric Univ. 5
Raybuck SA (1992) Microbes and microbial enzymes for cyanide degradation. Biodegradation 3:3–18
Aronstein BN, Maka A, Srivastava VJ (1994) Chemical and biological removal of cyanides from aqueous and soil-containing systems. Appl Microbiol Biotechnol 41:700–707
Gupta N, Balomajumder C, Agarwal VK (2010) Enzymatic mechanism and biochemistry for cyanide degradation: a review. J Hazard Mater 176:1–13. https://doi.org/10.1016/j.jhazmat.2009.11.038
Cabuk A, Taspinar A, Kolankaya UN (2006) Biodegration of cyanide by white rot fungus, Trametes versicolour. Biotechnol Lett 28:1313–1317
Angayarkanni J, Thandeeswaran M, Nisshanthini D, Karunya J, Palaniswamy M (2016) Prodigious action of microbes on poisonous ravage waste degradation. ENVIS News lett 14(1)
Tausigg A (1965) Some properties of induced enzyme cyanase. Can J Biochem 43:1063–1069
Castric PA, Strobel GA (1969) Cyanide metabolism by Bacillus megaterium. J Biol Chem 244:4089–4094
Dunnil PM, Fowden L (1965) Enzymatic formation of β-Cyanoalanine from cyanide by E-Coli extracts. Nature 208:1206–1207
Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 a resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669
Chena SC, Liu JK (1999) The respiratory responses to cyanide of a cyanide-resistant Klebsiella oxytoca bacterial strain. FEMS Microbiol Lett 175(1):37–43
Jensen P, Wilson MT, Aasa R, Malmström BG (1984) Cyanide inhibition of cytochrome c oxidase. A rapid-freeze epr investigation. Biochem J 224(3):829–837
Wagner AM, Krab K (1995) The alternative respiration pathway in plants: role and regulation. Physiol Plant 95:318–325. https://doi.org/10.1111/j.1399-3054.1995.tb00844.x
Siedow JN, Umbach AL (1995) Plant mitochondrial electron transfer and molecular biology. Plant Cell 7:821–831. https://doi.org/10.1105/tpc.7.7.821
Figueiredo H, Neves IC, Quintelas C, Tavares T, Taralung M, Mijoin J, Magnoux P (2006) Oxidation catalysts prepared from biosorbents supported on zeolites. Appl Catal B 66:274–280
Huertas MJ, Luque-Almagro VM, Martínez-Luque M, Blasco R, Moreno-Vivián C, Castillo F, Roldán MD (2006) Cyanide metabolism of Pseudomonas pseudoalcaligenes CECT5344: role of siderophores. Biochem Soc Trans 34:152–155
Kunz DA, Fernandez R, Parab P (2001) Evidence that bacterial cyanide oxygenase is a pterin dependenthydroxylase. Biochem Biophys Res Commun 281:514–518. https://doi.org/10.1006/bbrc.2001.5611
Fernandez RF, Dolghih E, Kunz DA (2004) Enzymatic assimilation of cyanide via pterin dependent oxygenolytic cleavage to ammonia and formate in Pseudomonas fluorescens NCIMB 11764. Appl Environ Microbiol 70:121–128. https://doi.org/10.1128/aem.70.1.121-128.2004
Durairaju Nisshanthini S, Teresa AK, Infanta SD, Raja S, Natarajan K, Palaniswamy M, Angayarkanni J (2014) Spectral characterization of a pteridine derivative from cyanide-utilizing bacterium Bacillus subtilis—JN989651. J Microbiol 53:262–271. https://doi.org/10.1007/s12275-015-4138-0
Mahendran R, Thandeeswaran M, Kiran G, Arulkumar M, Nawaz A, Jabastin J, Janani B, Thomas TA, Angayarkanni J (2018) Evaluation of pterin, a promising drug candidate from cyanide degrading bacteria. Curr Microbiol 75:684–693. https://doi.org/10.1007/s00284-018-1433-0
Kompis IM, Islam K, Then RL (2005) DNA and RNA synthesis: antifolates. Chem Rev 105:593–620. https://doi.org/10.1021/cr0301144
Ziegler SH, Harmsen R (1969) The biology of pteridine in insects. Adv Insect Physiol 6:139–203
Forrest HS, Van Baalen C (1970) Microbiology of unconjugated pteridines. Annu Rev Microbiol 24:91–108
Pimkov IV, Nigam A, Venna K, Fleming FF, Solntsev PV, Nemykin VN, Basu PJ (2013) Dithiolopyranthione synthesis, spectroscopy, and an unusual reactivity with DDQ. Heterocycl Chem 50:879–886
Dorsett D, Yim JJ, Jacobson KB (1979) Biosynthesis of “drosopterins” by an enzyme system from Drosophila melanogaster. Biochemistry 18:2596–2600. https://doi.org/10.1021/bi00579a025
Kritsky MS, Lyudnikova TA, Mironov EA, Moskaleva IVJ (1997) The UV radiation-driven reduction of pterins in aqueous solution. Photochem Photobiol B Biol 39:43–48. https://doi.org/10.1016/s1011-1344(96)07451-9
Thomas AH, Lorente C, Capparelli AL, Pokhhrel MR, Braun AM, Oliveros E (2002) Fluorescence of pterin 6-formylpterin, 6-carboxypterin and folic acid in aqueous solution: pH effects. Photochem Photobiol Sci 1:421–426. https://doi.org/10.1039/b202114e
Raemakers-Franken PC, Vanelderen CHM, Vanderdrift C, Vogels GD (1991) Identification of a novel tatiopterin derivative in methanogenium tationis. Bio-factors 3:127–130
Shanmuganathan MV, Krishnan S, Fu X, Prasadarao NV (2014) Escherichia coli K1 induces pterin production for enhanced expression of Fcg receptor I to invade RAW 264.7 macrophages. Microbes Infect 16:134–141. https://doi.org/10.1016/j.micinf.2013.10.013
Ikawa M, Sasner JJ, Haney JF, Foxall TL (1995) Pterins of the cyanobacterium Aphanizomenon flos-aquae. Phytochemistry 38(5):1229–1232
Cho SH, Na JU, Youn H, Hwang CS, Lee CH, Kang SO (1998) Tepidopterin, 1-O-(L-threo-biopterin-2′-yl)-β-N-acetylglucosamine from Chlorobium tepidum. Biochim Biophys Acta (BBA) Gen Subj 1379:53–60. https://doi.org/10.1016/s0304-4165(97)00081-0copbio.2015.12.004
Klein R, Thiery R, Tatischeff I (1990) Dictyopterin, 6-(d-threo-1, 2-dihydroxypropyl)-pterin, a new natural isomer of l-biopterin: isolation from vegetative cells of Dictyostelium discoideum and identification. Eur J Biochem 187:665–669. https://doi.org/10.1111/j.1432-1033.1990.tb15351
Basu P, Burgmayer SJ (2011) Pterin chemistry and its relationship to the molybdenum cofactor. NIH Public access 255:1016–1038. https://doi.org/10.1016/j.ccr.2011.02.010
Werner-Felmayer G, Golderer G, Werner ER (2002) Tetrahydrobiopterin biosynthesis, utilization and pharmacological effects. Curr Drug Metab 3:159–173. https://doi.org/10.2174/1389200024605073
Cronin SJ, Seehus C, Weidinger A, Talbot S, Reissig S, Seifert M, Kreslavsky T (2018) The metabolite BH4 controls T cell proliferation in autoimmunity and cancer. Nature. https://doi.org/10.1038/s41586-018-0701-2
Schwarz G (2005) Molybenum cofactor biosynthesis and deficiency. Cell Mol Life Sci 62:2792–2810
Hausen A, Bichler A, Fuchs D, Hetzel H, Reibnegger G, Watcher H (1985) Neopterin, a biochemical indicator of cellular immune reactions, in the detection and control of patients with neoplastic diseases. Cancer Detect Prev 8:121–128
Jackman AL, Taylor GA, O Connor BM, Bishop JA, Moran RG, Calvert AH (1990) Activity of the thymidylate synthase inhibitor 2-Desamino-N10-propargyl-5,8-dideazafolic acid and related compounds in murine (L1210) and human (W1L2) systems in Vitro and in L1210 in vivo. Cancer Res 50:5212–5218
Marques SM, Petushkov VN, Rodionova NS, Da Silva JC (2011) LC–MS and microscale NMR analysis of luciferin-related compounds from the bioluminescent earthworm Fridericia heliota. J Photochem Photobiol B 102:218–223. https://doi.org/10.1016/j.jphotobiol.2010.12.006
Hoffmann G, Schobersberger W (2004) Neopterin: a mediator of the cellular immune system. Pteridines 15:107–112
Wirleitner B, Schroecksnadel K, Winkler CH, Fuchs D (2005) Neopterin in HIV-1 infection. Mol Immun 42:183–194. https://doi.org/10.1016/j.molimm.2004.06.017
Gomtsyan A, Lee CH (2004) Nonnucleoside inhibitors of adenosine kinase. Curr Pharm Des 10:1093–1103. https://doi.org/10.2174/1381612043452703
Korkuryo Y, Nakatani T, Kakinuma M, Kabaki M, Kawata K, Kugimiya A (2000) New γ-fluoromethotrexates modified in the pteridine ring:synthesis and in vitro immunosuppressive activity. Eur J Med Chem 35:529–534
Shen C, Dillisen E, Kasran A, Lin Y, Herman J, Sienaert I, Jongheb S, Kerremans L, Geboes K, Boon L, Rutgeerts P, Ceuppens JL (2007) Immunosuppressive activity of a new pteridine derivative (4AZA1378) alleviates severity of TNBS—induced colitis in mice. Clin Immunol 122:53–61
Levenberg B, Hayaishi O (1959) A bacterial pterin deaminase. J Biol Chem 234:955–961
Peter JM, van Haaster T, Theo MK (1982) Signal transduction in the cellular slime molds. Mol Cell Endocrinol 26:1–17
Wernerfelmayer G, Golderer G, Werner ER, Grobner P, Wachter H (1994) Pteridine biosynthesis and nitric-oxide synthase in physarum-polycephalum. Biochem J 304:105–111
Goswami S, Maity AC, Fun H (2007) One-step synthesis of lumazine and xanthine: first co-crystal of lumazine and perchloric acid with a unique monohydrated hydronium ion (H5O2 +) mediated supramolecular assembly of the lumazine dimer. Eur J Org Chem. https://doi.org/10.1002/ejoc.200700271
Ziegler I, Mc Donald T, Hesslinger C, Pelletier I, Boyle P (2000) Development of the pteridine pathway in the Zebrafish Danio rerio. J Biochem 275:18926–18932. https://doi.org/10.1074/jbc.M910307199
Dumestre A, Chone T, Portal J, Gerard M, Berthelin J (1997) Cyanide degradation under alkaline conditions by a strain of Fusarium solani isolated from contaminated soils. Appl Environ Microbiol 63:2729–2734
Katayama Y, Narahara Y, Inoue Y, Amano F, Kanagawa T, Kuraishi H (1992) A thiocyanate hydrolase of Thiobacillus thioparus. A novel enzyme catalyzing the formation of carbonyl sulfide from thiocyanate. J Biol Chem 267:9170–9175
Ingvorsen K, Hajar-Pedersen B, Gotfredsen SE (1991) Novel cyanide hydrolysing enzyme from Alcaligenes xylosoxidans subsp denitrificans. Appl Environ Microbiol 57:1783–1789
Watanabe A, Yano K, Ikebukuro K, Karube I (1998) Cyanide hydrolysis in a cyanide-degrading bacterium, Pseudomonas stutzeri AK61, by cyanidase. Microbiology 144(6):1677–1682
Cipollone R, Ascenzi P, Tomao P, Imperi F, Visca P (2008) Enzymatic detoxification of cyanide: clues from Pseudomonas aeruginosa Rhodanese. J Mol Microbiol Biotechnol 15(2–3):199–211
Wang P, Vanettan HD (1992) cloning and properties of a cyanide hydratase gene from the phytopathogenic fungus Gloeocercospora sorghi. Biochem Biophys Res Commun 187:1048–1052
Atkinson A, Evans CGT, Yeo RG (1975) Behaviour of Bacillus stearothermophilus grown in different media. J Appl Bacteriol 38:301–303
Babu GRV, Wolfram JH, Chapatwala KD (1992) Conversion of sodium cyanide to carbon dioxide and ammonia by immobilised cells of Pseudomonas putida. J Ind Microbiol 9:235–238
Suh Y, Park JM, Yang J (1994) Biodegradation of cyanide compounds by Pseudomonas fluorescens immobilized on zeolite. Enzyme Microb Technol 16:529–533
Shivaraman N, Parhad NM (1985) Biodegradation of cyanide by Pseudomonas acidovorans and influence of pH and phenol. Indian J Environ Health 27:1–8
White DM, Schnabel W (1998) Treatment of cyanide waste in a sequencing batch biofilm reactor. Water Res 32:254–257
Kaewkannetra P, Imai T, Garcia GFJ, Chiu TY (2009) Cyanide removal from cassava mill wastewater using Azotobacter vinelandii TISTR 1094 with mixed microorganisms in activated sludge treatment system. J Hazard Mater 172:224–228. https://doi.org/10.1016/j.jhazmat.2009.06.162
Patil YB, Paknikar KM (2000) Development of a process for biodetoxification of metal cyanides from wastewaters. Proc Biochem 35:1139–1151
Paixao MA, Tavares CRG, Bergamasco R, Bonifacio ALE, Costa RT (2000) Anaerobic digestion from residue of industrial cassava industrialization with acidogenic and methanogenic physical separation phases. Appl Biochem Biotechnol 84–86:809–819
Sorokin DY, Tourova TP, Lysenko AM, Kuenen JG (2001) Microbial thiocyanate utilisation under highly alkaline conditions. Appl Biochem Microbiol 67:528–538. https://doi.org/10.1128/AEM.67.2.528-538.2001
Kwon HK, Woo SH, Park JM (2002) Thiocyanate degradation by Acremonium strictum and inhibition by secondary toxicants. Biotechnol Lett 24:1347–1351
Campos MG, Pereira P, Roseiro JC (2006) Packed-bed reactor for the integrated biodegradation of cyanide and formamide by immobilised Fusarium oxysporum CCMI 876 and Methylobacterium sp. RXM CCMI 908. Enzyme Microb Technol 38:848–854. https://doi.org/10.1016/j.enzmictec.2005.08.008
Maegala NM, Fridelina S, Abdullatif I (2011) Biodegradation of cyanide by Rhodococcus strains isolated in Malaysia. Int Conf Food Eng Biotechnol 9:21–25
Maegala NM, Fridelina S, Abdullatif I, Anthony EG (2012) Cyanide degradation by immobilised cells of Rhodococcus UKMP-5M. Biologia 67(5):837–844. https://doi.org/10.2478/s11756-012-0098-6
Karamba KI, Shukor MY, Syed MA, Zulkharnain A, Yasid NA, Khalil KA, Ahmad SA (2015) Isolation, screening and characterisation of cyanide degrading Serratia marcescens strain aq07. J Chem PharmbSci 8:401–406
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mahendran, R., BS, S., Thandeeswaran, M. et al. Microbial (Enzymatic) Degradation of Cyanide to Produce Pterins as Cofactors. Curr Microbiol 77, 578–587 (2020). https://doi.org/10.1007/s00284-019-01694-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-019-01694-9