Abstract
Industrial activity over the last two centuries has increased heavy metal contamination worldwide, leading to greater human exposure. Zinc is particularly common in industrial effluents and although an essential nutrient, it is highly toxic at elevated concentrations. Photoautotrophic microbes hold promise for heavy metal bioremediation applications because of their ease of culture and their ability to produce sulfide through metabolic processes that in turn are known to complex with the metal ion, Hg(II). The green alga Chlamydomonas reinhardtii, the red alga Cyanidioschyzon merolae, and the cyanobacterium Synechococcus leopoliensis were all able to synthesize sulfide and form zinc sulfide when exposed to Zn(II). Supplementation of their respective media with sulfite and cysteine had deleterious effects on growth, although ZnS still formed in Cyanidioschyzon cells to the same extent as in unsupplemented cells. The simultaneous addition of sulfate and Zn(II) had similar effects to that of Zn(II) alone in all three species, whereas supplying sulfate prior to exposure to Zn(II) enhanced metal sulfide production. The coupled activities of serine acetyltransferase and O-acetylserine(thiol)lyase (SAT/OASTL) did not increase significantly in response to conditions in which enhanced ZnS formation occurred; sulfate added prior to and simultaneously with Zn(II). However, even low activity could provide sufficient sulfate assimilation over this relatively long-term study. Because the extractable activity of cysteine desulfhydrase was elevated in cells that produced higher amounts of zinc sulfide, cysteine is the probable source of the sulfide in this aerobic process.
Similar content being viewed by others
References
Ahmad A, Mukherjee P, Mandal D, Senapati S, Khan MI, Kumar R, Sastry M (2002) Enzyme mediated extracellular synthesis of CdS nanoparticles by the fungus, Fusarium oxysporum. J Am Chem Soc 124:12108–12109
Allen MB (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32:270–277
Bai HJ, Zhang ZM, Guo Y, Yang GE (2009) Biosynthesis of cadmium sulfide nanoparticles by photosynthetic bacteria Rhodopseudomonas palustris. Coll Surf B: Biointerfaces 70:142–146
Bakels RHA, Vanwalraven HS, Vanwielink JE, Vanderzwetdegraaff I, Krenn BE, Krab K, Berden JA, Kraayenhof R (1994) The effect of sulfite on the ATP hydrolysis and synthesis activiyt of membrane-bound H+-ATP synthase from various species. biochemical and biophysical research communications. Biochem Biophys Res Commun 201:487–492
Behra R, Landwehrjohann R, Vogal L, Wagner B, Sigg L (2002) Copper and zinc content of periphyton from two rivers as a function of dissolved metal concentration. Aquat Sci 64:300–306
Chen J, Wu F, Wang W, Zheng C, Lin G, Dong X, He J, Pei Z, Zheng H (2011) Hydrogen sulphide enhances photosynthesis through promoting chloroplast biogenesis, photosynthetic enzyme expression, and thiol redox modification in Spinacia oleracea seedlings. J Exp Bot 62:4481–4493
Chu L, Ebersole J, Kurzban G, Holt S (1997) Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect Immun 65:3231–3238
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Ann Rev of Plant Biol 53:159–182
Dominguez M, Gutierrez F, Leon R, Vilchez C, Vega J, Vigara J (2003) Cadmium increases the activity levels of glutamate dehydrogenase and cysteine synthase in Chlamydomonas reinhardtii. Plant Physiol Biochem 41:828–832
Dominguez-Solis J, Lopez-Martin M, Ager F, Ynsa M, Romero L, Gotor C (2004) Increased cysteine availability is essential for cadmium tolerance and accumulation in Arabidopsis thaliana. Plant Biotech J 2:469–476
Gekeler W, Grill E, Winnacker E, Zenk MH (1988) Algae sequester heavy metals via synthesis of phytochelatin complexes. Arch Microbiol 150:197–202
Giordano M, Norici A, Hell R (2005) Sulfur and phytoplankton: acquisition, metabolism and impact on the environment. New Phytol 166:371–382
Gross W, Oesterhelt C (1999) Ecophysiological studies on red alga Galdieria sulphuraria isolated from southwest Iceland. Plant Biol 1:694–700
Gross W, Kuver J, Tischendorf G, Bouchaala N, Busch W (1998) Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur J Phycol 33:25–31
Groudeva VI, Groudev SN, Doycheva AS (2001) Bioremediation of waters contaminated with crude oil and toxic heavy metals. Int J Miner Process 62:293–299
Hancock JT, Lisjak M, Teklic T, Wilson ID, Whiteman M (2011) Hydrogen sulphide and signalling in plants. CAB Reviews: Perspectives in Agriculture, Veterinary Science. Nutr Nat Res 6:1–7
Hawkesford MJ, DeKok LJ (2006) Managing sulphur metabolism in plants. Plant Cell Environ 29:382–395
Holmes JD, Smith PR, Evans-Gowing R, Richardson DJ, Russell DA, Sodeau JR (1995) Energy-dispersive X-ray analysis of the extracellular cadmium sulfide crystallites of Klebsiella aerogenes. Arch Microbiol 163:143–147
Hong JS, Rabinowitz JC (1970) Molar extinction coefficient and iron and sulfide content of clostridial ferredoxin. J Biol Chem 245:4982–4987
Hrabak E, Chan C, Gribskov M, Harper J, Choi J, Halford N, Kudla J, Luan S, Nimmo H, Sussman M, Thomas M, Walker-Simmons K, Zhu J, Harmon A (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases RID B-3872-2009. Plant Physiol 132:666–680
Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182
Kawashima CG, Noji M, Nakamura M, Ogra Y, Suzuki KT, Saito K (2004) Heavy metal tolerance of transgenic tobacco plants over-expressing cysteine synthase. Biotechnol Lett 26:153–157
Kelly DJA, Budd K, Lefebvre DD (2007) Biotransformation of mercury in pH-stat cultures of eukaryotic freshwater algae. Arch Microbiol 187:45–53
Kelly D, Budd K, Lefebvre DD (2006) Mercury analysis of acid- and alkaline-reduced biological samples: identification of meta-cinnabar as the major biotransformed compound in algae. Appl Environ Microbiol 72:361–367
Kertesz MA (2001) Bacterial transporters for sulfate and organosulfur compounds. Res Microbiol 152:279–290
Kimura H (2011) Hydrogen sulfide: its production, release and functions. Amino Acids 41:113–121
Kopriva S (2006) Regulation of sulfate assimilation in arabidopsis and beyond. Ann Bot 97:479–495
Lefebvre DD, Edwards CD (2010) Decontaminating heavy metals using photosynthetic microbes. In: Shaw V (ed) Emerging environmental technologies, IIth edn. Springer, New York, pp 57–73
Lefebvre DD, Kelly D, Budd K (2007) Biotransformation of Hg(II) by cyanobacteria. Appl Environ Microbiol 73:243–249
Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–644
Lyons T, Gasch A, Gaither L, Botstein D, Brown P, Eide D (2000) Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc Natl Acad Sci U S A 97:7957–7962
MacDiarmid C, Gaither L, Eide D (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19:2845–2855
Maret W (2003) Cellular zinc and redox states converge in the metallothionein/thionein pair. J Nutr 133:1460S–1462S
Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima S, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657
Melis A, Chen H (2005) Chloroplast sulfate transport in green algae—genes, proteins and effects. Photosynthesis Res 86:299–307
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu L, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen C, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral J, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen C, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WCA, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR, Chlamydomonas Annotation JGI, Team A (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions RID A-3530-2008 RID A-1214-2009 RID A-1755-2010 RID C-1537-2010. Science 318:245–251
Mikolajczyk M, Awotunde O, Muszynska G, Klessig D, Dobrowolska G (2000) Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165–178
Miller B, Heuser T, Zimmer W (1999) A Synechococcus leopoliensis SAUG 1402–1 operon harboring the 1-deoxyxylulose 5-phosphate synthase gene and two additional open reading frames is functionally involved in the dimethylallyl diphosphate synthesis. FEBS Lett 460:485–490
Moriarty-Craige S, Jones D (2004) Extracellular thiols and thiol/disulfide redox in metabolism. Annu Rev Nutr 24:481–509
Mosulen S, Dominguez M, Vigara J, Vilchez C, Guiraum A, Vega J (2003) Metal toxicity in Chlamydomonas reinhardtii: Effect on sulfate and nitrate assimilation. Biomol Eng 20:199–203
Murasugi A, Wada C, Hayashi Y (1983) Occurrence of acid-labile sulfide in cadmium-binding peptide 1 from fission yeast. J Biochem 93:661–664
Muyzer G, Stams AJM (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454
Niknahad H, O’Brien PJ (2008) Mechanism of sulfite cytotoxicity in isolated rat hepatocytes. Chem Biol Interact 174:147–154
Ning H, Zhang C, Yao Y, Yu D (2010) Overexpression of a soybean O-acetylserine (thiol) lyase-encoding gene GmOASTL4 in tobacco increases cysteine levels and enhances tolerance to cadmium stress. Biotech Letters 32:557–564
Nozaki H, Toda K, Takano H, Kuroiwa T (2001) The second serine acetyltransferase, bacterial-type O-acetylserine (thiol) lyase and eukaryotic-type O-acetylserine (thiol) lyase from the primitive red alga Cyanidioschyzon merolae. J Plant Res 114:291–300
Papenbrock J, Riemenschneider A, Kamp A, Schulz-Vogt H, Schmidt A (2007) Characterization of cysteine-degrading and H2S-releasing enzymes of higher plants—from the field to the test tube and back. Plant Biol 9:582–588
Perales-Vela HV, Peña-Castro JM, Cañizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64:1–10
Pinto G, Albertano P, Ciniglia C, Cozzolino S, Pollio A, Yoon H, Bhattacharya D (2003) Comparative approaches to the taxonomy of the genus Galdieria merola (Cyanidiales, Rhodophyta). Cryptogam Algol 24:13–32
Pollock SV, Pootakham W, Shibagaki N, Moseley JL, Grossman AR (2005) Insights into the acclimation of Chlamydomonas reinhardtii to sulfur deprivation. Photosynth Res 86:475–489
Rabinowitch H, Fridovich I (1985) Growth of Chlorella sorokiniana in the presence of sulfite elevates cell content of superoxide dismutase and imparts resistance towards paraquat. Planta 164:524–528
Rabinowitz JC (1978) [30] Analysis of acid-labile sulfide and sulfhydryl groups. In: Anonymous Methods in Enzymology. Academic, pp 275–277
Ravina CG, Barroso C, Vega JM, Gotor C (1999) Cysteine biosynthesis in Chlamydomonas reinhardtii. Molecular cloning and regulation of O-acetylserine(thiol)lyase. Eur J Biochem 264:848–853
Reese RN, White CA, Winge DR (1992) Cadmium-sulfide crystallites in Cd-(γEC)nG peptide complexes from tomato. Plant Physiol 98:225–229
Rennenberg H (1983) Role of O-Acetylserine in hydrogen sulfide emission from pumpkin leaves in response to sulfate. Plant Physiol 73:560–565
Rijstenbil JW, Derksen WJ, Gerringa LJA, Poortvliet TCW, Sandee A, van den Berg M, van Drie J, Wijnholds JA (1994) Oxidative stress induced by copper: defense and damage in the marine planktonic diatom Ditylum brightwellii, grown in continuous cultures with high and low zinc levels. Mar Biol 119:583–590
Rippka R, Waterbury J, Cohen-Bazire G (1974) A cyanobacterium which lacks thylakoids. Arch Microbiol 100:419–436
Robinson N (1989) Algal metallothioneins: secondary metabolites and proteins. J Appl Phycol 1:5–18
Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiol 136:2443–2450
Scarano G, Morelli E (2003) Properties of phytochelatin-coated CdS nanocrystallites formed in a marine phytoplanktonic alga (Phaeodactylum tricornutum, Bohlin) in response to Cd. Plant Science 165:803–810
Sekiya J, Schmidt A, Wilson LG, Filner P (1982) Emission of hydrogen sulfide by leaf tissue in response to l-cysteine. Plant Physiol 70:430–436
Siegel LM (1965) A direct microdetermination for sulfide. Anal Biochem 11:126–132
Smith FW, Hawkesford MJ, Prosser IM, Clarkson DT (1995) Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high affinity sulphate transporter at the plasma membrane. Mol Gen Genet 247:709–715
Speiser DM, Abrahamson SL, Banuelos G, Ow DW (1992) Brassica juncea produces a phytochelatin–cadmium–sulfide complex. Plant Physiol 99:817–821
Stauber J, Florence T (1987) Mechanism of toxicity of ionic copper and copper-complexes to algae. Mar Biol 94:511–519
Sueoka N, Chiang KS, Kates JR (1967) Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardi I. Isotopic transfer experiments with a strain producing eight zoospores. J Mol Biol 25:47–66
Sweeney RY, Mao C, Gao X, Burt JL, Belcher AM, Georgiou G, Iverson BL (2004) Bacterial biosynthesis of cadmium sulfide nanocrystals. Chem Biol 11:1553–1559
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, JdA E, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci U S A 94:11102–11107
Tsuji N, Nishikori S, Iwabe O, Shiraki K, Miyasaka H, Takagi M, Hirata K, Miyamoto K (2004) Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120. Biochem Biophys Res Commun 315:751–755
Wang CL, Lum AM, Ozuna SC, Clark DS, Keasling JD (2001) Aerobic sulfide production and cadmium precipitation by Escherichia coli expressing the Treponema denticola cysteine desulfhydrase gene. Appl Microbiol Biotechnol 56:425–430
Wang C, Maratukulam P, Lum A, Clark D, Keasling J (2000) Metabolic engineering of an aerobic sulfate reduction pathway and its application to precipitation of cadmium on the cell surface. Appl Environ Microbiol 66:4497–4502
Wilson LG, Bressan RA, Filner P (1978) Light-dependent emission of hydrogen sulfide from plants. Plant Physiol 61:184–189
Acknowledgments
This research was supported by Natural Sciences and Engineering Council of Canada and the Advisory Research Committee of Queen’s University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Edwards, C.D., Beatty, J.C., Loiselle, J.B.R. et al. Aerobic transformation of zinc into metal sulfide by photosynthetic microorganisms. Appl Microbiol Biotechnol 97, 3613–3623 (2013). https://doi.org/10.1007/s00253-012-4636-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-012-4636-5