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New insights into the genetic and metabolic diversity of thiocyanate-degrading microbial consortia

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Abstract

Thiocyanate is a common contaminant of the gold mining and coal coking industries for which biological degradation generally represents the most viable approach to remediation. Recent studies of thiocyanate-degrading bioreactor systems have revealed new information on the structure and metabolic activity of thiocyanate-degrading microbial consortia. Previous knowledge was limited primarily to pure-culture or co-culture studies in which the effects of linked carbon, sulfur and nitrogen cycling could not be fully understood. High throughput sequencing, DNA fingerprinting and targeted gene amplification have now elucidated the genetic and metabolic diversity of these complex microbial consortia. Specifically, this has highlighted the roles of key consortium members involved in sulfur oxidation and nitrification. New insights into the biogeochemical cycling of sulfur and nitrogen in bioreactor systems allow tailoring of the microbial metabolism towards meeting effluent composition requirements. Here we review these rapidly advancing studies and synthesize a conceptual model to inform new biotechnologies for thiocyanate remediation.

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References

  • Aguirre NV, Vivas BP, Montes-Morán MA, Ania CO (2010) Adsorption of thiocyanate anions from aqueous solution onto adsorbents of various origin. Adsorpt Sci Technol 28(8):705–716

    Article  CAS  Google Scholar 

  • Akcil A (2003) Destruction of cyanide in gold mill effluents: biological versus chemical treatments. Biotechnol Adv 21(6):501–511 doi:http://dx.doi.org/. doi:10.1016/S0734-9750(03)00099-5

    Article  PubMed  CAS  Google Scholar 

  • Anderson PM (1980) Purification and properties of the inducible enzyme cyanase. Biochemistry 19(13):2882–2888

    Article  PubMed  CAS  Google Scholar 

  • Anderson PM, Y-c S, Fuchs JA (1990) The cyanase operon and cyanate metabolism. FEMS Microbiol Rev 7(3–4):247–252

    Article  PubMed  CAS  Google Scholar 

  • Banerjee G (1996) Phenol-and thiocyanate-based wastewater treatment in RBC reactor. J Environ Eng 122(10):941–948

    Article  CAS  Google Scholar 

  • Beller HR, Chain PS, Letain TE, Chakicherla A, Larimer FW, Richardson PM, Coleman MA, Wood AP, Kelly DP (2006) The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 188(4):1473–1488

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Betts P, Rinder D, Fleeker J (1979) Thiocyanate utilization by an arthrobacter. Can J Microbiol 25(11):1277–1282

    Article  PubMed  CAS  Google Scholar 

  • Bezsudnova EY, Sorokin DY, Tikhonova TV, Popov VO (2007) Thiocyanate hydrolase, the primary enzyme initiating thiocyanate degradation in the novel obligately chemolithoautotrophic halophilic sulfur-oxidizing bacterium Thiohalophilus thiocyanoxidans. BBA-Proteins Proteom 1774(12):1563–1570

    Article  CAS  Google Scholar 

  • Bhunia F, Saha N, Kaviraj A (2000) Toxicity of thiocyanate to fish, plankton, worm, and aquatic ecosystem. Bull Environ Contam Toxicol 64(2):197–204

    Article  PubMed  CAS  Google Scholar 

  • Breuer P, Jeffery C, Meakin R (2011) Fundamental investigations of the SO2/air, peroxide and Caro’s acid cyanide destruction processes. In: Proceedings of ALTA 2011 Gold Conference. ALTA Metallurgical Services, Perth, pp. 154–168

    Google Scholar 

  • Dash RR, Gaur A, Balomajumder C (2009) Cyanide in industrial wastewaters and its removal: a review on biotreatment. J Hazard Mater 163(1):1–11

    Article  PubMed  Google Scholar 

  • du Plessis C, Barnard P, Muhlbauer R, Naldrett K (2001) Empirical model for the autotrophic biodegradation of thiocyanate in an activated sludge reactor. Lett Appl Microbiol 32(2):103–107

    Article  PubMed  Google Scholar 

  • Ebbs S (2004) Biological degradation of cyanide compounds. Curr Opin Biotechnol 15(3):231–236 doi:http://dx.doi.org/. doi:10.1016/j.copbio.2004.03.006

    Article  PubMed  CAS  Google Scholar 

  • Felföldi T, Székely AJ, Gorál R, Barkács K, Scheirich G, András J, Rácz A, Márialigeti K (2010) Polyphasic bacterial community analysis of an aerobic activated sludge removing phenols and thiocyanate from coke plant effluent. Bioresour Technol 101(10):3406–3414

    Article  PubMed  Google Scholar 

  • Gould WD, King M, Mohapatra BR, Cameron RA, Kapoor A, Koren DW (2012) A critical review on destruction of thiocyanate in mining effluents. Miner Eng 34:38–47

    Article  Google Scholar 

  • Happold F, Jones G, Pratt D (1958) Utilization of thiocyanate by Thiobacillus thioparus and T. thiocyanoxidans. Nature 182:266–267

    Article  PubMed  CAS  Google Scholar 

  • Huddy RJ, van Zyl AW, van Hille RP, Harrison ST (2015) Characterisation of the complex microbial community associated with the ASTER™ thiocyanate biodegradation system. Miner Eng 76:65–71

    Article  CAS  Google Scholar 

  • Hussain A, Ogawa T, Saito M, Sekine T, Nameki M, Matsushita Y, Hayashi T, Katayama Y (2013) Cloning and expression of a gene encoding a novel thermostable thiocyanate-degrading enzyme from a mesophilic alphaproteobacteria strain THI201. Microbiology 159(Pt 11):2294–2302

    Article  PubMed  CAS  Google Scholar 

  • Jensen JN, Tuan Y-J (1993) Chemical oxidation of thiocyanate ion by ozone. Ozone-Sci Eng 15(4):343–360

    Article  CAS  Google Scholar 

  • Kantor RS, Zyl AW, Hille RP, Thomas BC, Harrison ST, Banfield JF (2015) Bioreactor microbial ecosystems for thiocyanate and cyanide degradation unravelled with genome-resolved metagenomics. Environ Microbiol. doi:10.1111/1462-2920.12936

    Google Scholar 

  • Katayama Y, Kuraishi H (1978) Characteristics of Thiobacillus thioparus and its thiocyanate assimilation. Can J Microbiol 24(7):804–810

    Article  PubMed  CAS  Google Scholar 

  • 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(13):9170–9175

    PubMed  CAS  Google Scholar 

  • Katayama Y, Hiraishi A, Kuraishi H (1995) Paracoccus thiocyanatus sp. nov., a new species of thiocyanate-utilizing facultative chemolithotroph, and transfer of Thiobacillus versutus to the genus Paracoccus as Paracoccus versutus comb. nov. with emendation of the genus. Microbiology 141(6):1469–1477

    Article  PubMed  CAS  Google Scholar 

  • Katayama Y, Matsushita Y, Kaneko M, Kondo M, Mizuno T, Nyunoya H (1998) Cloning of genes coding for the three subunits of thiocyanate hydrolase of Thiobacillus thioparus THI 115 and their evolutionary relationships to nitrile hydratase. J Bacteriol 180(10):2583–2589

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kelly DP, Baker SC (1990) The organosulphur cycle: aerobic and anaerobic processes leading to turnover of C1-sulphur compounds. FEMS Microbiol Rev 7(3–4):241–246

    Article  Google Scholar 

  • Kelly DP, Wood AP (2000) Confirmation of Thiobacillus denitrificans as a species of the genus Thiobacillus, in the beta-subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. Int J Syst Evol Microbiol 50(2):547–550

    Article  PubMed  Google Scholar 

  • Kim S-J, Katayama Y (2000) Effect of growth conditions on thiocyanate degradation and emission of carbonyl sulfide by Thiobacillus thioparus THI115. Water Res 34(11):2887–2894

    Article  CAS  Google Scholar 

  • Kim S-W, Fushinobu S, Zhou S, Wakagi T, Shoun H (2009) Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion? Appl Environ Microbiol 75(9):2652–2658

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kwon HK, Woo SH, Park JM (2002) Thiocyanate degradation by Acremonium strictum and inhibition by secondary toxicants. Biotechnol Lett 24(16):1347–1351

    Article  CAS  Google Scholar 

  • Lee C, Kim J, Chang J, Hwang S (2003) Isolation and identification of thiocyanate utilizing chemolithotrophs from gold mine soils. Biodegradation 14(3):183–188

    Article  PubMed  CAS  Google Scholar 

  • Lee C, Kim J, Do H, Hwang S (2008) Monitoring thiocyanate-degrading microbial community in relation to changes in process performance in mixed culture systems near washout. Water Res 42(4–5):1254–1262 doi:http://dx.doi.org/. doi:10.1016/j.watres.2007.09.017

    Article  PubMed  CAS  Google Scholar 

  • Mudder TI, Botz M, Smith A (2001) Chemistry and treatment of cyanidation wastes. Mining Journal Books, London

    Google Scholar 

  • Ogawa T, Noguchi K, Saito M, Nagahata Y, Kato H, Ohtaki A, Nakayama H, Dohmae N, Matsushita Y, Odaka M (2013) Carbonyl sulfide hydrolase from Thiobacillus thioparus strain THI115 is one of the β-carbonic anhydrase family enzymes. J Am Chem Soc 135(10):3818–3825

    Article  PubMed  CAS  Google Scholar 

  • Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P, von Bergen M, Lagkouvardos I, Karst SM, Galushko A, Koch H (2015) Cyanate as an energy source for nitrifiers. Nature 524(7563):105–108

    Article  PubMed  CAS  Google Scholar 

  • Patil Y (2014) Development of a bioremediation technology for the removal of thiocyanate from aqueous industrial wastes using metabolically active microorganisms. In: Patil YB, Rao P (eds) Applied bioremediation-active and passive approaches. Intech Open Science, Croatia

  • Ryu B-G, Kim W, Nam K, Kim S, Lee B, Park MS, Yang J-W (2015) A comprehensive study on algal–bacterial communities shift during thiocyanate degradation in a microalga-mediated process. Bioresour Technol 191:496–504

    Article  PubMed  CAS  Google Scholar 

  • Shoji T, Sueoka K, Satoh H, Mino T (2014) Identification of the microbial community responsible for thiocyanate and thiosulfate degradation in an activated sludge process. Process Biochem 49(7):1176–1181

    Article  CAS  Google Scholar 

  • Sorokin DY, Tourova TP, Lysenko AM, Kuenen JG (2001) Microbial thiocyanate utilization under highly alkaline conditions. Appl Environ Microbiol 67(2):528–538

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sorokin DY, Tourova TP, Lysenko AM, Mityushina LL, Kuenen JG (2002) Thioalkalivibrio thiocyanoxidans sp. nov. and Thioalkalivibrio paradoxus sp. nov., novel alkaliphilic, obligately autotrophic, sulfur-oxidizing bacteria capable of growth on thiocyanate, from soda lakes. Int J Syst Evol Microbiol 52(2):657–664

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Antipov AN, Muyzer G, Kuenen JG (2004) Anaerobic growth of the haloalkaliphilic denitrifying sulfur-oxidizing bacterium Thialkalivibrio thiocyanodenitrificans sp. nov. with thiocyanate. Microbiology 150(7):2435–2442

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Abbas B, van Zessen E, Muyzer G (2014) Isolation and characterization of an obligately chemolithoautotrophic Halothiobacillus strain capable of growth on thiocyanate as an energy source. FEMS Microbiol Lett 354(1):69–74

    Article  PubMed  CAS  Google Scholar 

  • Stafford D, Callely A (1969) The utilization of thiocyanate by a heterotrophic bacterium. J Gen Microbiol 55(2):285–289

    Article  PubMed  CAS  Google Scholar 

  • Staib C, Lant P (2007) Thiocyanate degradation during activated sludge treatment of coke-ovens wastewater. Biochem Eng J 34(2):122–130

    Article  CAS  Google Scholar 

  • Stott M, Franzmann P, Zappia L, Watling H, Quan L, Clark B, Houchin M, Miller P, Williams T (2001) Thiocyanate removal from saline CIP process water by a rotating biological contactor, with reuse of the water for bioleaching. Hydrometallurgy 62(2):93–105

    Article  CAS  Google Scholar 

  • Stratford J, Dias AEO, Knowles CJ (1994) The utilization of thiocyanate as a nitrogen source by a heterotrophic bacterium: the degradative pathway involves formation of ammonia and tetrathionate. Microbiology 140(10):2657–2662

    Article  PubMed  CAS  Google Scholar 

  • van Hille RP, Dawson E, Edward C, Harrison ST (2015) Effect of thiocyanate on BIOX® organisms: inhibition and adaptation. Minerals Engineering 75:110–115

    Article  Google Scholar 

  • van Zyl AW, Harrison ST, van Hille RP (2011) Biodegradation of thiocyanate by a mixed microbial population. Mine Water–Managing the Challenges (IMWA 2011), Aachen

  • van Zyl AW, Huddy R, Harrison STL, van Hille RP (2014) Evaluation of the ASTER™ process in the presence of suspended solids. Minerals Engineering doi:http://dx.doi.org/. doi:10.1016/j.mineng.2014.11.007

    Google Scholar 

  • Villemur R, Juteau P, Bougie V, Ménard J, Déziel E (2015) Development of four-stage moving bed biofilm reactor train with a pre-denitrification configuration for the removal of thiocyanate and cyanate. Bioresour Technol 181:254–262

    Article  PubMed  CAS  Google Scholar 

  • Vu H, Mu A, Moreau J (2013) Biodegradation of thiocyanate by a novel strain of burkholderia phytofirmans from soil contaminated by gold mine tailings. Lett Appl Microbiol 57(4):368–372

    PubMed  CAS  Google Scholar 

  • Wald MH, Lindberg HA, Barker MH (1939) The toxic manifestations of the thiocyanates. J Am Med Assoc 112(12):1120–1124

    Article  CAS  Google Scholar 

  • Whitlock JL (1990) Biological detoxification of precious metal processing wastewaters. Geomicrobiol J 8(3–4):241–249

    Article  CAS  Google Scholar 

  • Wilson I, Harris G (1960) The oxidation of thiocyanate ion by hydrogen peroxide. I. The pH-independent reaction. J Am Chem Soc 82(17):4515–4517

    Article  CAS  Google Scholar 

  • Wood AP, Kelly DP, McDonald IR, Jordan SL, Morgan TD, Khan S, Murrell JC, Borodina E (1998) A novel pink-pigmented facultative methylotroph, Methylobacterium thiocyanatum sp. nov., capable of growth on thiocyanate or cyanate as sole nitrogen sources. Arch Microbiol 169(2):148–158

  • Yamasaki M, Matsushita Y, Namura M, Nyunoya H, Katayama Y (2002) Genetic and immunochemical characterization of thiocyanate-degrading bacteria in lake water. Appl Environ Microbiol 68(2):942–946

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Youatt JB (1954) Studies on the metabolism of Thiobacillus thiocyanoxidans. J Gen Microbiol 11(2):139–149

    Article  PubMed  CAS  Google Scholar 

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Correspondence to John W. Moreau.

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Watts, M.P., Moreau, J.W. New insights into the genetic and metabolic diversity of thiocyanate-degrading microbial consortia. Appl Microbiol Biotechnol 100, 1101–1108 (2016). https://doi.org/10.1007/s00253-015-7161-5

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