Biological degradation of cyanide compounds

Stephen Ebbs
Cyanide compounds are produced as waste products of a number of industrial processes and several routes for their removal from the environment are under investigation, including the use of biodegradation. The most recent developments in this area have come from studies of the hydrolytic and oxidative pathways for biodegradation and the conditions that affect their activity. The biodegradation of cyanide under anaerobic conditions has also recently demonstrated the feasibility for concomitant biogas generation, a possible economic benet of the process. Signicant advances have been reported in the use of plants for the phytoremediation of cyanide compounds and evidence for the biodegradation of thiocyanate and metalcyanide complexes has become available. Despite these advances, however, physical and economic factors still limit the application of cyanide biodegradation, as do competing technologies.
Addresses Department of Plant Biology, Southern Illinois University Carbondale, 420 Life Science II, Mailcode 6509, 1125 Lincoln Drive, Carbondale, Illinois 62901, USA e-mail: sebbs@plant.siu.edu

Degradation pathways are sensitive to the form and concentration of the cyanide compound, the physicochemical conditions of the media, and the presence of interfering and inhibitory compounds. The development of biodegradation strategies for these varied conditions requires a comprehensive understanding of the biological pathways. Presented here are recent studies of these pathways, along with a brief discussion of current advances in the development of cyanide-related biotechnologies. Limiting factors for these biotechnologies are also discussed.

Biodegradation of free cyanide and nitriles

There are four general pathways for the biodegradation of cyanide: hydrolytic; oxidative; reductive; and substitution/transfer (Figure 1). Several reviews have described these pathways and the organisms in which they are found [35]. Nevertheless, additional organisms with the capacity for cyanide biodegradation are still being reported [6,79]. More than one pathway can be utilized for cyanide biodegradation in some organisms [3,10]; the pathway used is dictated by the external conditions such as oxygen, pH and cyanide concentration. Cyanide bioavailability and solubility in soilwater systems are also determining factors [11]. Hydrolytic reactions are catalyzed by cyanide hydratase, forming formamide, or cyanidase, which produces formate and ammonia (Figure 1). Cyanide hydratase is primarily a fungal enzyme and is highly conserved between species [12]. Cyanidase (cyanide dihydratase) is principally bacterial. Cyanide hydratase and cyanidase have recently been shown to have similarity at both the amino acid and structural levels to nitrilase and nitrile hydratase enzymes [13]. Nitrile-utilizing enzymes have been found in a wide variety of bacterial, fungal and plant species. Nitrilases and nitrile hydratases convert both aliphatic and aromatic nitriles to the corresponding acid or amide, respectively, but show less substrate specicity than cyanide hydratase and cyanidase. For example, transformation of Escherichia coli with the cyanide hydratase gene from Fusarium lateritium allowed for growth on nitriles as the sole nitrogen source. Site-directed mutagenesis of this gene abolished both cyanide hydratase and nitrilase activity, suggesting that cyanide hydratase also possesses nitrilase activity [14]. The diversity of enzymes in this superfamily and their varied catalytic activity and substrate specicities presents considerable opportunity for biotechnological development, including the bioremediation of industrial nitrile wastes [15,16]. Two yeast strains, Cryptococcus sp. UFMG-Y28 and Candida guilliermondii CCT 7207, were able to use nitriles such as
Current Opinion in Biotechnology 2004, 15:231236

Current Opinion in Biotechnology 2004, 15:231236 This review comes from a themed issue on Environmental biotechnology Edited by Michael Y Galperin and Alan JM Baker Available online 15th April 2004 0958-1669/$ see front matter 2004 Elsevier Ltd. All rights reserved. DOI 10.1016/j.copbio.2004.03.006

Introduction
Cyanide played a principle role in the evolution of life on Earth [1] and remains an important form of nitrogen for microorganisms, fungi and plants. Although some organisms synthesize cyanide, a greater number are capable of cyanide biodegradation. The existence of these pathways has allowed the development of biotechnologies to degrade cyanide compounds in industrial waste streams. Major sources of cyanide discharges include petrochemical rening, the synthesis of organic chemical and plastics, electroplating, aluminum works, the former manufactured gas industry, and metal mining and processing industries. The release of cyanide from these industries has been estimated to be >14 million kg yr1 [2]. Cyanide can be present in environmental matrices and waste streams as simple cyanides (e.g. HCN, CN, NaCN), metal cyanide complexes, cyanates and nitriles.
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232 Environmental biotechnology

Figure 1

Hydrolytic reactions Cyanide hydratase HCN + H2O HCONH2 Nitrile hydratase R-CN + H2O R-CONH2 Cyanidase HCN + 2H2O HCOOH Nitrilase R-CN + 2H2O R-COOH Chemical reactions for the biodegradation of cyanide and thiocyanate Oxidative reactions Cyanide monoxygenase HCN + O2 + H+ + NAD(P)H HOCN + NAD(P)+ + H2O Cyanide dioxygenase HCN + O2 + 2H+ + NAD(P)H CO2 + NH3 + NAD(P)+ Substitution/transfer reactions Cyanoalanine synthase Cysteine + CN -cyanoalanine + H2S OAS + CN -cyanoalanine + CH3COO Thiosulfate:cyanide sulfurtransferase CN + S2O32 SCN + SO32

Reductive reactions HCN + 2H+ + 2e CH2=NH + H2O CH2=O CH2=NH + 2H+ + 2e CH3-NH + 2H+ + 2e CH4 + NH3

Thiocyanate biodegradation Carbonyl pathway (thiocyanate hydrolase) SCN + 2H2O COS + NH3 + OH Cyanate pathway (cyanase) SCN + 3H2O + 2O2 CNO + HS HS + 2O2 SO42 + H+ CNO + 3H+ + HCO3 NH4+ + 2CO2
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The general categories of chemical reactions responsible for the biodegradation of cyanide and thiocyanate. For the hydrolytic reaction involving nitriles, R represents either an aliphatic or aromatic group. The substitution/transfer reaction catalyzed by cyanoalanine synthase can also use O-acetylserine (OAS) as a substrate. The cyanate formed by cyanide monoxygenase is converted to NH4 and CO2 by the same pathway as the cyanate from thiocyanate. The reductive pathway is derived from the action of nitrogenase and the products resulting from the transfer of pairs of electrons.

benzonitrile as the sole nitrogen source for growth. Biodegradation by C. guilliermondii CCT 7207 was more effective when the cells were immobilized [15], an observation that reiterates earlier studies showing that immobilized organisms or enzymes provide an effective platform for cyanide biodegradation. Nitrile biodegradation is further inuenced by the cyanide concentration in the system. Biodegradation of acrylonitrile by Bacillus subtilis produced increasing levels of cyanide in the media, which in turn initiated the autolysis of the bacteria [17]. This is an important observation, because it indicates that if the rate of nitrile hydrolysis exceeds the subsequent rate of cyanide biodegradation then a sustained biodegradation system cannot be maintained unless additional organisms are included to biodegrade the cyanide formed. One possibility would be to combine nitrilase activity with that of b-cyanoalanine synthase (Figure 1), one of the substitution/transfer pathways [3]. The cyanoalanine is then converted to
Current Opinion in Biotechnology 2004, 15:231236

asparagine by cyanoalanine hydrolase or possibly by asparaginase. Despite this suggestion, there appears to have been no recent effort to develop this combined approach or an approach based solely upon the substitution/transfer reactions. The oxidative reactions for the biodegradation of cyanide form ammonia and carbon dioxide (Figure 1). Cyanide monoxygenase converts cyanide to cyanate, with cyanase then catalyzing the bicarbonate-dependent conversion of cyanate to ammonia and carbon dioxide. Cyanases, which have been identied in numerous bacteria, fungi, plants and animals [18], have been the principle focus of study. The presumed role of cyanase has long been as a protection against cyanate poisoning [3]. As cyanate is not a common metabolite, more fundamental roles for cyanases in bicarbonate/carbon dioxide and nitrogen metabolism have been proposed. Additional suggested roles for plant cyanases include ammonia assimilation following cyanate
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Biological degradation of cyanide compounds Ebbs 233

biodegradation and a role in the concentration and delivery of carbon dioxide for photosynthesis [18]. These speculative roles rely heavily upon the assumption that cyanate arises at a sufcient rate, such as through the degradation of urea and the nucleotide precursor carbamoyl phosphate. If these results are substantiated, then additional emphasis might need to be placed upon the biological role of cyanate and its biodegradation. The biodegradation of thiocyanate and selenocyanate has also been studied (Figure 1). Thiocyanate is used in a variety of chemical processes and can be produced from the reaction of cyanide with pyretic materials in waste streams. Thiocyanate is produced in vivo by the action of thiosulfate-cyanide sulfurtransferase enzymes (Figure 1); biodegradation of thiocyanate can occur by at least two pathways [19,2022]. Three species of thiocyanateutilizing bacteria, isolated from highly alkaline soda lake sediments and soils, formed large amounts of cyanate when grown at pH 10 with thiocyanate as the nitrogen source. Cyanase activity was also high, converting the cyanate to ammonia and carbon dioxide [21]. The fungi Acremonium strictum produced ammonia and sulfate from thiocyanate without the production of cyanate [19]. The authors contend their results argue against a cyanate pathway, but the formation of sulfate is consistent with the proposed cyanate pathway [20,21]. In a second pathway, thiocyanate is converted to ammonia and carbonyl sulde. Evidence for this carbonyl pathway comes from the identication of the enzyme responsible (thiocyanate hydrolase) in the chemolithotroph Thiobacillus thioparus and genes encoding this enzyme have been identied in other thiocyanate-degrading bacterial cultures [22]. This hydrolase shows a signicant homology at the amino acid level to nitrile hydratases. Selenocyanate, a pollutant produced by oil reneries, power plants and cyanide leaching of selenide ores, can be degraded by plants, but it is has not been determined whether this occurs via a cyanate or thiocyanate hydrolase pathway [23]. As industrial activities are likely to increase thiocyanate and selenocyanate levels in the environment, the biodegradation pathways for these compounds warrant additional study. A second oxidative pathway utilizes cyanide dioxygenase to form ammonia and carbon dioxide directly (Figure 1). Recently, the requirement for a pterin cofactor in this reaction has been proposed [24]. Additionally, in E. coli strain BCN6 and P. uorescens NCIMB 11764, the formation of cyanohydrin complexes was reportedly necessary for oxygenase-mediated cyanide biodegradation [25,26]. Whether or not complexation is obligatory for cyanide biodegradation via oxygenase activity has yet to be established, however. Formation of these keto acids was proposed to be a more generalized pathway employed by organisms for cyanide tolerance and utilization [25] and might therefore provide an important key
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to maximizing oxygenase-mediated cyanide biodegradation, particularly as bacterial growth decreases as cyanide concentration increases.

Biodegradation of metal cyanide complexes

Perhaps the greatest need with respect to cyanide biodegradation is biodegradation of metal cyanide complexes. Cyanide can complex with Fe, Au, Cd, Co, Cu and Ni, with the Fe and Au complexes being the most stable. Iron cyanides are the dominant CN species in soil and groundwater [27], with total CN concentrations in contaminated media as high as 4% by weight [28,29]. As Fe is a ubiquitous element in soils and aquifers, equilibrium favors the formation of complexes such as ferrocyanide [Fe(CN)64] and ferricyanide [Fe(CN)63]. The strong complexes formed between cyanide and precious metals have been utilized for decades in ore heap leaching operations to selectively extract gold from low grade ores. This approach creates large volumes of cyanide-laden solutions that must be subsequently treated. These metalcyanide complexes show greater resistance to biodegradation than simple cyanides. Cyanide complexes with Fe dissociate slowly in the dark, but undergo rapid photolysis in the presence of UV light to yield free cyanide. This complicates efforts to remediate metal cyanide complexes in the subsurface and makes the laboratory study of their biodegradation more difcult. Ironically, countries like the United States regulate simple cyanide and thiocyanate, but not metal cyanide complexes. Metal cyanide complexes in waste streams can be treated by current biotechnologies, yet there is little emphasis on the remediation of iron cyanides in the environment because of their lower toxicity and presumed stability. The few exceptions are those industries that have an economic interest in the removal of these compounds or those that practice good environmental stewardship. Reports of metalcyanide complex biodegradation have been present in the literature for nearly as long as reports of cyanide biodegradation. Recent studies [6,8,28,30,31] reiterate these observations, suggesting that known cyanide-degrading organisms such as P. uorescens and F. solani also biodegrade Fe and Ni complexes with cyanide. The metabolism of both simple cyanides and iron cyanide complexes by plants has also been reported [32,33,34]. A potential shortcoming of these studies, however, is the lack of proper controls for light and the spontaneous dissociation of the metal cyanide complexes. Few studies have taken steps to control light or to monitor cyanide speciation to account for dissociation [30,35]. Several report that biodegradation products of metal cyanide complexes include ammonia or formamide. In the absence of proper controls, it is difcult to ascertain whether the organisms present were using the metal cyanides directly or whether biodegradation acted solely upon the dissociated free cyanide. Although perhaps a
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subtle distinction, it is nonetheless important because it may indicate that the biodegradation of metalcyanide complexes is a function of the dissociation of the complex, rather than the biological degradation of the cyanide complex. Nevertheless, the large-scale biological treatment of waste streams containing cyanide, metal cyanides and thiocyanate has been underway at several sites, including the recently closed Homestake Mine operation. The 48 rotating reactors at Homestake processed a reported 5.5 million gallons of inuent per day with 95% removal of cyanide [3]. A study with willow (Salix eriocephala) did control light and monitored cyanide speciation in both the presence and absence of the plant to provide more conclusive evidence of plant-mediated metabolism of ferrocyanide. Specically, the study showed that the dissociation of ferrocyanide to free cyanide could not account for the mass of ferrocyanide lost from the system [32]. Additional research with plants, bacteria and fungi is needed to provide conclusive evidence of metal cyanide biodegradation. The studies with plants are particularly encouraging, because they suggest that phytoremediation of simple cyanide and ironcyanide complexes might be a feasible biotechnology for in situ remediation, as was reported for at least one site in Denmark [33].

tase (chy) in F. solani has been sequenced and primers utilized in reverse transcription-polymerase chain reaction (RTPCR) to demonstrate transcription of this gene. The chy gene from F. solani displays signicant homology to the corresponding cyanide hydratase gene from Gloeocercospora sorghi, F. lateritium and Leptosphaeria maculans. This observation implies that the assay could be utilized in different contexts, provided that expression of the chy gene can be conclusively linked with activity of cyanide hydratase. This assay, if sufciently robust, could provide an important tool to site managers, regulators and industries that generate cyanide wastes.

Conclusions
The continued development and application of biotechnologies for cyanide biodegradation is limited primarily by physical and economic factors. Most organisms capable of biodegrading cyanide are sensitive to cyanide concentration, with biodegradation and/or growth rate decreasing above specic thresholds for each organism. Solutions containing cyanide concentrations of up to 100 mg L1 can be treated, although a commercially marketed strain of Fusarium displaying high levels of cyanide hydratase activity can reportedly treat cyanide concentrations of up to 10 000 mg L1 [3]. As efuents from some industries can have concentrations above the maximum range for most organisms, biological treatment may not be a viable option in all cases. The formation of degradation products, such as ammonia, or the presence of other nitrogen sources (e.g. nitrate and nitrite) or contaminants (e.g. phenol) may also limit the efcacy with which some waste streams can be treated. In addition, the pH of these waste streams might limit cyanide biodegradation. Cyanide hydrolysis has an optimal pH range of 7 to 9, whereas thiocyanate biodegradation can occur at pH 10. As the efciency of cyanide biodegradation decreases outside of these ranges, not all waste streams may be amenable to biological treatment. From an economic standpoint, biological treatment options might not be as cost-effective as chemical methods for cyanide destruction, particularly for industries that lack the infrastructure to develop biological treatment systems. There is also an increasing emphasis on cyanide recovery, as opposed to treatment, as well as a suggestion that cyanogenic microorganisms such as Chromobacterium violaceum can be grown directly on ore surfaces to provide localized cyanide biogenesis for metal extraction [41]. The future of cyanide biodegradation technologies will hinge on their ability to compete with these technologies or to ll specic needs associated with the treatment of industrial efuents. Valueadded benets, such as economic return gained from biogas production, might also promote interest. In situ biotechnologies such as phytoremediation could provide an additional niche for the treatment of cyanide compounds, if subsequent research supports the efcacy of this approach.
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Recent advances in cyanide biodegradation technologies

Two bioreactor studies with wastewater have renewed the focus on reductive processes (Figure 1) during anaerobic cyanide biodegradation [36,37]. One advantage of these anaerobic bioreactors is that cyanide biodegradation can support the growth of methanogens, suggesting a possible productive use for biogas generation. Methanogenesis from anaerobic biogranules was inhibited by increasing cyanide concentrations [37], however, so the cyanide concentration in the feedstock may be a limiting factor. A separate study, which used a bioreactor fed with processing wastes from the cyanogenic plant cassava, showed that the methanogens present were limited to the genus Methanothrix [36]. The identication of additional genera that can produce methane in the presence of cyanide may help drive the development of this technology. Studies of aerobic cyanide biodegradation also continue, with one describing the development of a portable batch system designed specically for cold regions [38]. Two other studies demonstrated that combined anaerobicaerobic reactor systems were also capable of signicant cyanide biodegradation [39,40], with one also lowering phenol and ammonia concentrations of a simulated wastewater to below regulatory limits [40]. One novel study has proposed a transcription-based assay for monitoring the biodegradation of both simple and metal cyanides [12]. The gene encoding cyanide hydraCurrent Opinion in Biotechnology 2004, 15:231236

Biological degradation of cyanide compounds Ebbs 235

Update
Bacterial strains from the genus Klebsiella have been shown to degrade both cyanide and thiocyanate. Strains of Klebsiella oxytoca isolated from cyanide-enriched industrial wastewaters grew on cyanide as the sole nitrogen source [42]. In the presence of cyanide, resting cell cultures produced methane and showed increased activity of nitrogenase, suggesting a reductive pathway for cyanide biodegradation. However, while no formate or formamide were detected in the cell cultures following cyanide treatment, resting cell cultures incubated in the presence of cyanide readily degraded both compounds when present in the media within 8 h. This is suggestive of an oxidative pathway for cyanide biodegradation. These contrasting observations raise questions about the pathway(s) involved in cyanide biodegradation by K. oxytoca and whether the pathway utilized depends upon the presence or absence of oxygen in the system. With respect to thiocyanate, seven bacterial strains isolated from the soil surrounding a gold mine in Korea were shown to biodegrade thiocyanate (initial concentration 150 mg L1) within 16 days [43]. The seven strains identied included one strain of Corynebacterium nitrilophilus, four from the genus Bacillus, and two from the genus Brevibacterium. A phylogenetic analysis using 16S rDNA from the strain identied initially as Brevibacterium epidermidis revealed that the strain was more closely related to members of the genus Klebsiella. This reportedly provided the rst evidence of chemoautolithotrophic use of thiocyanate by a strain of Klebsiella. If thiocyanate biodegradation in Klebsiella occurs via the carbonyl pathway, it is conceivable that nitrogenase activity might not only contribute to cyanide biodegradation [42], but might also indirectly contribute to thiocyanate degradation by removing the carbonyl sulde formed by thiocyanate hydrolase.

Metabolite identication was carried out to determine the biodegradation products of the nickel cyanide complex, with the results reportedly showing the rst evidence that a cyanide complex can be used as the sole nitrogen source for growth. 7. Sexton AC, Howlett BJ: Characterisation of a cyanide hydratase gene in the phytopathenogenic fungus Leptosphaeria maculans. Mol Gen Genet 2000, 263:463-470. Yanese H, Sakamoto A, Okamoto K, Kita K, Sato Y: Degradation of the metal-cyano complex tetracyanonickelate (II) by Fusarium oxysporum N-10. Appl Biochem Microbiol 2000, 53:328-334. Adjei MD, Ohta Y: Isolation and characterization of a cyanideutilizing Burkholderia cepacia strain. World J Microbiol Biotechnol 1999, 15:699-704.

8.

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10. Ezzi-Mufaddal I, Lynch James M: Cyanide catabolizing enzymes in Trichoderma spp. Enzyme Microb Technol 2002, 31:1042-1047. 11. Aronstein BN, Maka A, Srivastava VJ: Chemical and biological removal of cyanides from aqueous and soil-containing systems. Appl Biochem Microbiol 1994, 41:700-707. 12. Barclay M, Day JC, Thompson IP, Knowles CJ, Bailey MJ:  Substrate-regulated cyanide hydratase (chy) gene expression in Fusarium solani: the potential of a transcription-based assay for monitoring the biotransformation of cyanide complexes. Environ Microbiol 2002, 4:183-189. A transcription-based assay for the fungal gene encoding cyanide hydratase is proposed as a means of monitoring cyanide biodegradation. 13. OReilly C, Turner PD: The nitrilase family of CN hydrolysing  enzymes a comparative study. J Appl Microbiol 2003, 95:1161-1174. This thorough review provides a summary of the nitrilase enzyme superfamily, which includes both cyanidase and cyanide hydratase. The article includes discussions of enzyme structure and substrate specicity as well as the results of a molecular genetic analysis of the family. 14. Nolan LM, Harnedy PA, Turner P, Hearne AB, OReilly C: The cyanide hydratase enzyme of Fusarium lateritium has nitrilase activity. FEMS Microbiol Lett 2003, 221:161-165. 15. Rezende RP, Dias JCT, Ferraz V, Linardi VR: Metabolism of benzonitrile by Cryptococcus sp. UFMG-Y28. J Basic Microbiol 2000, 40:389-392. 16. Dias JCT, Rezende RP, Linardi VR: Bioconversion of nitriles by Candida guilliermondii CCT 7207 cells immobilized in barium alginate. Appl Microbiol Biotechnol 2001, 56:757-761. 17. Reyes GF, Corbett D, Benz FW, Doyle RJ: Acrylonitrile induces autolysis Bacillus subtilis. FEMS Microbiol Lett 2000, 182:255-258. 18. Guilloton M, Espie GS, Anderson PM: What is the role of cyanase  in plants? Rev Plant Biochem Biotechnol 2002, 1:57-79. The authors provide a review of the enzyme cyanase in bacteria, fungi and plants, with an emphasis on the role played by this enzyme, particularly in plants. A phylogenetic analysis of cyanases is provided along with accession numbers for nearly all sequences discussed. 19. Kwon HK, Woo SH, Park JM: Thiocyanate degradation by  Acremonium strictum and inhibition by secondary toxicants. Biotechnol Lett 2002, 24:1347-1351. The authors report on the biodegradation of thiocyanate by Acremonium strictum and include data describing the concentration dependence of biodegradation and the inhibition caused by other compounds that can be present in industrial waste streams, such as phenol, nitrate, nitrite and ammonia. 20. du Plessis CA, Barnard P, Muhlbauer RM, Naldrett K: Empirical model for the autotrophic biodegradation of thiocyanate in an activated sludge reactor. Lett Appl Microbiol 2001, 32:103-107. 21. Sorokin DY, Tourova TP, Lysenko AM, Kuenen JG: Microbial thiocyanate utilization under highly alkaline conditions. Appl Biochem Microbiol 2001, 67:528-538. 22. Yamasaki M, Matsushita Y, Namura M, Nyunoya H, Katayama Y: Genetic and immunochemical characterization of thiocyanate-degrading bacteria in lake water. Appl Biochem Microbiol 2002, 68:942-946. Current Opinion in Biotechnology 2004, 15:231236

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:  of special interest  of outstanding interest 1. J, Lazcano-Araujo A: The role of HCN and its derivatives in Oro prebiotic evolution. In Cyanide in Biology. Edited by Vennesland B, Conn EE, Knowles CJ, Westley J, Wissing F: London: Academic Press; 1981:517-541. ATSDR: Toxicological Prole for Cyanide. Atlanta, GA: US Department of Health Human Services, Public Health Service; 1997. Raybuck SA: Microbes and microbial enzymes for cyanide degradation. Biodegradation 1992, 3:3-18. Knowles CJ, Bunch AW: Microbial cyanide metabolism. Adv Microb Physiol 1986, 27:73-111. Dubey SK, Holmes DS: Biological cyanide destruction mediated by microorganisms. World J Microbiol Biotechnol 1995, 11:257.

2.

3. 4. 5. 6. 

Kwon HK, Woo SH, Park JM: Degradation of tetracyanonickelate (II) by Cryptococcus humicolus MCN2. FEMS Microbiol Lett 2002, 214:211-216. The authors describe the characterization of a new yeast strain, Cryptococcus humicolus, capable of degrading nickel cyanide complexes. www.sciencedirect.com

236 Environmental biotechnology

23. de Souza MP, Pickering IJ, Walla M, Terry N: Selenium  assimilation and volatilization from selenocyanate-treated Indian mustard and muskgrass. Plant Physiol 2002, 128:625-633. Perhaps the only study addressing the possible biodegradation of selenocyanate, this study showed that two plant species could degrade this compound, volatilizing the liberated selenium. This study demonstrates the possibility of selenocyanate phytoremediation. 24. Kunz DA, Fernandez RF, Parab P: Evidence that bacterial cyanide oxygenase is a pterin-dependent hydroxylase. Biochem Biophys Res Commun 2001, 287:514-518. 25. Kunz DA, Chen JL, Pan G: Accumulation of a-keto acids as essential components in cyanide assimilation by Pseudomonas uorescens NCIMB 11764. Appl Biochem Microbiol 1998, 64:4452-4459. 26. Figueira MM, Ciminelli VST, de Andrade MC, Linardi VR: Cyanide degradation by an Escherichia coli strain. Can J Microbiol 1996, 42:519-523. 27. Meeussen JL, Keizer MG, Van Riemsdijk WH: Dissolution behavior of iron cyanide (prussian blue) in contaminated soils. Environ Sci Technol 1992, 26:1832-1838. 28. Barclay M, Tett VA, Knowles CJ: Metabolism and enzymology of cyanide/metallocyanide biodegradation by Fusarium solani under neutral and acidic conditions. Enzyme Microb Technol 1998, 23:321-330. 29. Theis TL, Young TC, Huang M, Knutsen KC: Leachate characteristics and composition of cyanide-bearing wastes from manufactured gas plants. Environ Sci Technol 1994, 28:99-106. 30. Dursun AY, Calik A, Aksu Z: Degradation of ferrous(II) cyanide complex ions by Pseudomonas uorescens. Process Biochem 1999, 34:901-908. 31. Barclay M, Hart A, Knowles CJ, Meeussen JCL, Tett VA: Biodegradation of metal cyanides by mixed and pure cultures of fungi. Enzyme Microb Technol 1998, 22:223-231. 32. Ebbs SD, Bushey J, Poston S, Kosma D, Samiotakis M,  Dzombak D: Transport and metabolism of free cyanide and iron cyanide complexes by willow. Plant Cell Environ 2003, 26:1467-1478. Using stringent controls and chemical speciation analyses, this study showed that willow plants were capable of transporting and metabolizing

ferrocyanide, an iron cyanide complex. This study demonstrated the possible application of phytoremediation to iron cyanide contamination. 33. Trapp S, Larsen M, Christiansen H: Experimente zum verbleib von cyanid nach aufnahme in panzen. Umwelt Schad Forsch 2001, 13:29-37. [Translation: Experimental data on the kinetics of the degradation of cyanide after uptake in plants.] 34. Trapp S, Koch I, Christiansen H: Aufnahme von cyanid in panzen: risiko oder chance fuer die phytoremediation? Umwelt Schad Forsch 2001, 13:20-28. [Translation: Uptake of cyanides in plants: risk or chance for phytoremediation?] 35. Cherryholmes KL, Cornils WJ, McDonald B, Splinter R: Biological degradation on complex iron cyanides in natural aquatic systems. In 7th Symposium on Aquatic Toxicology and Hazard Assessment Aptil 17-19; Milwaukee, WI: Edited by Cardwell RD, Purdy R, Bahner RC: 1983:502-511. 36. Paixao MA, Tavares CRG, Bergamasco R, Bonifacio ALE, 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. 37. Annachhatre AP, Amornkaew A: Toxicity and degradation of cyanide in batch methanogenesis. Environ Technol 2000, 21:135-145. 38. White DM, Pilon TA, Woolard C: Biological treatment of cyanide containing wastewater. Water Res 2000, 34:2105-2109. 39. Oliveira MA, Reis EM, Nozaki J: Biological treatment of wastewater from the cassava meal industry. Environ Res 2001, 85:177-183. 40. Chakraborty S, Veeramani H: Anaerobic-anoxic-aerobic sequential degradation of synthetic wastewaters. Appl Biochem Biotechnol 2002, 102-103:443-451. 41. Campbell SC, Olson GJ, Clark TR, McFeters G: Biogenic production of cyanide and its application to gold recovery. J Ind Microbiol Biotechnol 2001, 26:134-139. 42. Kao CM, Liu JK, Lou HR, Lin CS, Chen SC: Biotransformation of cyanide to methane and ammonia by Klebsiella oxytoca. Chemosphere 2003, 50:1055-1061. 43. Lee C, Kim J, Chang J, Hwang S: Isolation and identication of thiocyanate utilizing chemolithotrophs from gold mine soils. Biodegradation 2003, 14:183-188.

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