Site-directed mutagenesis of HgcA and HgcB reveals amino acid residues important for mercury methylation

Applied and Environmental Microbiology

Volumn 81, Issue 9, 2015, Pages 3205-3217

  Smith, Steven D ^a   Bridou, Romain ^a,e   Johs, Alexander ^b   Parks, Jerry M ^c   Elias, Dwayne A ^c,d   Hurt, Richard A ^c   Brown, Steven D ^c,d   Podar, Mircea ^b,d   Wall, Judy D ^a  

^a University of Missouri   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

^e UNIVERSITÉ DE PAU ET DES PAYS DE L'ADOUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; AMINO ACIDS; COBALT; ENCODING (SYMBOLS); GENES; LIGANDS; MERCURY (METAL); PROTEINS;

AMINO ACID RESIDUES; ANAEROBIC MICROORGANISMS; CONSERVED RESIDUES; DESULFOVIBRIO DESULFURICANS; INORGANIC MERCURY; MERCURY METHYLATION; METHYLATION CAPACITY; SITE DIRECTED MUTAGENESIS;

METHYLATION;

AMINO ACID; METHYLMERCURY; MUTAGENICITY; TOXIN;

DESULFOVIBRIO DESULFURICANS;

AMINO ACID; BACTERIAL PROTEIN; MERCURY; METHYLMERCURY DERIVATIVE; MUTANT PROTEIN;

CONSERVED SEQUENCE; DESULFOVIBRIO DESULFURICANS; DNA MUTATIONAL ANALYSIS; ENZYMOLOGY; GENETICS; METABOLISM; SITE DIRECTED MUTAGENESIS;

AMINO ACIDS; BACTERIAL PROTEINS; CONSERVED SEQUENCE; DESULFOVIBRIO DESULFURICANS; DNA MUTATIONAL ANALYSIS; MERCURY; METHYLMERCURY COMPOUNDS; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS;

EID: 84927794402     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00217-15     Document Type: Article

References (61)

1. Wood JM. 1974. Biological cycles for toxic elements in the environment. Science 183:1049-1052. http://dx.doi.org/10.1126/science.183.4129.1049.
2. Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N. 2013. Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967-4983. http://dx.doi.org/10.1021/es305071v.
3. Lamborg CH, Hammerschmidt CR, Bowman KL, Swarr GJ, Munson KM, Ohnemus DC, Lam PJ, Heimburger L-E, Rijkenberg MJA, Saito MA. 2014. A global ocean inventory of anthropogenic mercury based on water column measurements. Nature 512:65-68. http://dx.doi.org/10.1038/nature13563.
4. Hintelmann H. 2010. Organomercurials. Their formation and pathways in the environment. Met Ions Life Sci 7:365-401. http://dx.doi.org/10.1039/BK9781847551771-00365.
5. Harris RC, Rudd JW, Amyot M, Babiarz CL, Beaty KG, Blanchfield PJ, Bodaly RA, Branfireun BA, Gilmour CC, Graydon JA, Heyes A, Hintelmann H, Hurley JP, Kelly CA, Krabbenhoft DP, Lindberg SE, Mason RP, Paterson MJ, Podemski CL, Robinson A, Sandilands KA, Southworth GR, St Louis VL, Tate MT. 2007. Whole-ecosystem study shows rapid fishmercury response to changes in mercury deposition. Proc Natl Acad SciUSA 104:16586-16591. http://dx.doi.org/10.1073/pnas.0704186104.
6. Vazquez M, Velez D, Devesa V. 2014. In vitro characterization of the intestinal absorption of methylmercury using a Caco-2 cell model. Chem Res Toxicol 27:254-264. http://dx.doi.org/10.1021/tx4003758.
7. Gilmour CC, Henry EA, Mitchell R. 1992. Sulfate stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281-2287. http://dx.doi.org/10.1021/es00035a029.
8. Compeau GC, Bartha R. 1985. Sulfate-reducing bacteria: principal methylators of mercury in anoxic estuarine sediment. Appl Environ Microbiol 50:498-502.
9. Hamelin S, Amyot M, Barkay T, Wang Y, Planas D. 2011. Methanogens: principal methylators of mercury in lake periphyton. Environ Sci Technol 45:7693-7700. http://dx.doi.org/10.1021/es2010072.
10. Yu RQ, Reinfelder JR, Hines ME, Barkay T. 2013. Mercury methylation by the methanogen Methanospirillum hungatei. Appl Environ Microbiol 79:6325-6330. http://dx.doi.org/10.1128/AEM.01556-13.
11. Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD, Somenahally AC, Johs A, Hurt RA, Jr, Bailey KL, Elias DA. 2013. Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810-11820. http://dx.doi.org/10.1021/es403075t.
12. Parks JM, Johs A, Podar M, Bridou R, Hurt RA, Jr, Smith SD, Tomanicek SJ, Qian Y, Brown SD, Brandt CC, Palumbo AV, Smith JC, Wall JD, Elias DA, Liang L. 2013. The genetic basis for bacterial mercury methylation. Science 339:1332-1335. http://dx.doi.org/10.1126/science.1230667.
13. Choi SC, Bartha R. 1993. Cobalamin-mediated mercury methylation by Desulfovibrio desulfuricans LS. Appl Environ Microbiol 59:290-295.
14. Choi SC, Chase T, Jr, Bartha R. 1994. Enzymatic catalysis of mercury methylation by Desulfovibrio desulfuricans LS. Appl Environ Microbiol 60:1342-1346.
15. Choi SC, Chase T, Bartha R. 1994. Metabolic pathways leading to mercury methylation in Desulfovibrio desulfuricans LS. Appl Environ Microbiol 60:4072-4077.
16. Berman M, Chase T, Bartha R. 1990. Carbon flow in mercury biomethylation by Desulfovibrio desulfuricans. Appl Environ Microbiol 56:298-300.
17. Goetzl S, Jeoung JH, Hennig SE, Dobbek H. 2011. Structural basis for electron and methyl-group transfer in a methyltransferase system operating in the reductive acetyl-CoA pathway. J Mol Biol 411:96-109. http://dx.doi.org/10.1016/j.jmb.2011.05.025.
18. Svetlitchnaia T, Svetlitchnyi V, Meyer O, Dobbek H. 2006. Structural insights into methyltransfer reactions of a corrinoid iron-sulfur protein involved in acetyl-CoA synthesis. Proc Natl Acad Sci U S A 103:14331-14336. http://dx.doi.org/10.1073/pnas.0601420103.
19. Bae HS, Dierberg FE, Ogram A. 2014. Syntrophs dominate sequences associated with the mercury methylation-related gene hgcA in the water conservation areas of the Florida Everglades. Appl Environ Microbiol 80: 6517-6526. http://dx.doi.org/10.1128/AEM.01666-14.
20. Liu YR, Yu RQ, Zheng YM, He JZ. 2014. Analysis of the microbial community structure by monitoring an Hg methylation gene (hgcA) in paddy soils along an Hg gradient. Appl Environ Microbiol 80:2874-2879. http://dx.doi.org/10.1128/AEM.04225-13.
21. Schaefer J, Kronberg RM, Morel F, Skyllberg U. 2014. Detection of a key Hg methylation gene, hgcA, in wetland soils. Environ Microbiol Rep 6:441-447. http://dx.doi.org/10.1111/1758-2229.12136.
22. Ando N, Kung Y, Can M, Bender G, Ragsdale SW, Drennan CL. 2012. Transient B12-dependent methyltransferase complexes revealed by smallangle X-ray scattering. J Am Chem Soc 134:17945-17954. http://dx.doi.org/10.1021/ja3055782.
23. Ljungdahl LG, LeGall J, Lee JP. 1973. Isolation of a protein containing tightly bound 5-methoxybenzimidazolylcobamide (factor 3m) from Clostridium thermoaceticum. Biochemistry 12:1802-1808. http://dx.doi.org/10.1021/bi00733a022.
24. Kung Y, Ando N, Doukov TI, Blasiak LC, Bender G, Seravalli J, Ragsdale SW, Drennan CL. 2012. Visualizing molecular juggling within a B12-dependent methyltransferase complex. Nature 484:265-269. http://dx.doi.org/10.1038/nature10916.
25. Doukov T, Seravalli J, Stezowski JJ, Ragsdale SW. 2000. Crystal structure of a methyltetrahydrofolate-and corrinoid-dependent methyltransferase. Structure 8:817-830. http://dx.doi.org/10.1016/S0969-2126(00)00172-6.
26. Ragsdale SW. 2008. Catalysis of methyl group transfers involving tetrahydrofolate and B12. Vitam Horm 79:293-324. http://dx.doi.org/10.1016/S0083-6729(08)00410-X.
27. Banerjee R, Ragsdale SW. 2003. The many faces of vitamin B12: catalysis by cobalamin-dependent enzymes. Annu Rev Biochem 72:209-247. http://dx.doi.org/10.1146/annurev.biochem.72.121801.161828.
28. Hennig SE, Jeoung J-H, Goetzl S, Dobbek H. 2012. Redox-dependent complex formation by an ATP-dependent activator of the corrinoid/ironsulfur protein. Proc Natl Acad Sci U S A 109:5235-5240. http://dx.doi.org/10.1073/pnas.1117126109.
29. Ferguson T, Soares JA, Lienard T, Gottschalk G, Krzycki JA. 2009. RamA, a protein required for reductive activation of corrinoid-dependent methylamine methyltransferase reactions in methanogenic archaea. J Biol Chem 284:2285-2295. http://dx.doi.org/10.1074/jbc.M807392200.
30. Zhou J, Riccardi D, Beste A, Smith JC, Parks JM. 2014. Mercury methylation by HgcA: theory supports carbanion transfer to Hg(II). Inorg Chem 53:772-777. http://dx.doi.org/10.1021/ic401992y.
31. Bertini I, Donaire A, Feinberg BA, Luchinat C, Piccioli M, Yuan H. 1995. Solution structure of the oxidized 2[4Fe-4S] ferredoxin from Clostridium pasteurianum. Eur J Biochem 232:192-205. http://dx.doi.org/10.1111/j.1432-1033.1995.tb20799.x.
32. Davy SL, Osborne MJ, Moore GR. 1998. Determination of the structure of oxidised Desulfovibrio africanus ferredoxin I by 1H NMR spectroscopy and comparison of its solution structure with its crystal structure. J Mol Biol 277:683-706. http://dx.doi.org/10.1006/jmbi.1998.1631.
33. Bruschi M, Hatchikian EC. 1982. Non-heme iron proteins of Desulfovibrio: the primary structure of ferredoxin I from Desulfovibrio africanus. Biochimie 64:503-507. http://dx.doi.org/10.1016/S0300-9084(82)80166-1.
34. Gilmour CC, Elias DA, Kucken AM, Brown SD, Palumbo AV, Schadt CW, Wall JD. 2011. Sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 as a model for understanding bacterial mercury methylation. Appl Environ Microbiol 77:3938-3951. http://dx.doi.org/10.1128/AEM.02993-10.
35. Zane GM, Yen H-CB, Wall JD. 2010. Effect of the deletion of qmoABC and the promoter-distal gene encoding a hypothetical protein on sulfate reduction in Desulfovibrio vulgaris Hildenborough. Appl Environ Microbiol 76:5500-5509. http://dx.doi.org/10.1128/AEM.00691-10.
36. Li MZ, Elledge SJ. 2012. SLIC: a method for sequence-and ligationindependent cloning. Methods Mol Biol 852:51-59. http://dx.doi.org/10.1007/978-1-61779-564-0_5.
37. Magis C, Taly JF, Bussotti G, Chang JM, Di Tommaso P, Erb I, Espinosa-Carrasco J, Notredame C. 2014. T-Coffee: tree-based consistency objective function for alignment evaluation. Methods Mol Biol 1079:117-129. http://dx.doi.org/10.1007/978-1-62703-646-7_7.
38. Shapiro AL, Vinuela E, Maizel JV, Jr. 1967. Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem Biophys Res Commun 28:815-820. http://dx.doi.org/10.1016/0006-291X(67)90391-9.
39. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350-4354.
40. Burnette WN. 1981. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 112:195-203.
41. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
42. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685. http://dx.doi.org/10.1038/227680a0.
43. Ragsdale SW, Lindahl PA, Munck E. 1987. Mossbauer, EPR, and optical studies of the corrinoid/iron-sulfur protein involved in the synthesis of acetyl coenzyme A by Clostridium thermoaceticum. J Biol Chem 262: 14289-14297.
44. Morrison KL, Weiss GA. 2001. Combinatorial alanine-scanning. Curr Opin Chem Biol 5:302-307. http://dx.doi.org/10.1016/S1367-5931(00)00206-4.
45. von Heijne G. 1991. Proline kinks in transmembrane alpha-helices. J Mol Biol 218:499-503. http://dx.doi.org/10.1016/0022-2836(91)90695-3.
46. Nilsson I, Saaf A, Whitley P, Gafvelin G, Waller C, von Heijne G. 1998. Proline-induced disruption of a transmembrane alpha-helix in its natural environment. J Mol Biol 284:1165-1175. http://dx.doi.org/10.1006/jmbi.1998.2217.
47. DeSilva TM, Veglia G, Porcelli F, Prantner AM, Opella SJ. 2002. Selectivity in heavy metal-binding to peptides and proteins. Biopolymers 64:189-197. http://dx.doi.org/10.1002/bip.10149.
48. Carugo O, Cemazar M, Zahariev S, Hudaky I, Gaspari Z, Perczel A, Pongor S. 2003. Vicinal disulfide turns. Protein Eng 16:637-639. http://dx.doi.org/10.1093/protein/gzg088.
49. Wouters MA, Fan SW, Haworth NL. 2010. Disulfides as redox switches: from molecular mechanisms to functional significance. Antioxid Redox Signal 12:53-91. http://dx.doi.org/10.1089/ars.2009.2510.
50. Matthews RG. 2009. Cobalamin-and corrinoid-dependent enzymes. Met Ions Life Sci 6:53-114. http://dx.doi.org/10.1039/BK9781847559159-00053.
51. Ludwig ML, Matthews RG. 1997. Structure-based perspectives on B12-dependent enzymes. Annu Rev Biochem 66:269-313. http://dx.doi.org/10.1146/annurev.biochem.66.1.269.
52. Guimarães DH, Weber A, Klaiber I, Vogler B, Renz P. 1994. Guanylcobamide and hypoxanthylcobamide-corrinoids formed by Desulfovibrio vulgaris. Arch Microbiol 162:272-276. http://dx.doi.org/10.1007/BF00301850.
53. Matthews RG. 2001. Cobalamin-dependent methyltransferases. Acc Chem Res 34:681-689. http://dx.doi.org/10.1021/ar0000051.
54. Ferry JG. 1993. Fermentation of acetate, p 304-334. In Ferry JG (ed), Methanogenesis: ecology, physiology, biochemistry & genetics. Chapman & Hall, New York, NY.
55. Iismaa SE, Vazquez AE, Jensen GM, Stephens PJ, Butt JN, Armstrong FA, Burgess BK. 1991. Site-directed mutagenesis of Azotobacter vinelandii ferredoxin I. Changes in [4Fe-4S] cluster reduction potential and reactivity. J Biol Chem 266:21563-21571.
56. Lafrance-Vanasse J, Lefebvre M, Di Lello P, Sygusch J, Omichinski JG. 2009. Crystal structures of the organomercurial lyase MerB in its free and mercury-bound forms: insights into the mechanism of methylmercury degradation. J Biol Chem 284:938-944. http://dx.doi.org/10.1074/jbc.M807143200.
57. Pitts KE, Summers AO. 2002. The roles of thiols in the bacterial organomercurial lyase (MerB). Biochemistry 41:10287-10296. http://dx.doi.org/10.1021/bi0259148.
58. Sorokin DY, Tourova TP, Mussmann M, Muyzer G. 2008. Dethiobacter alkaliphilus gen. nov. sp. nov., and Desulfurivibrio alkaliphilus gen. nov. sp. nov.: two novel representatives of reductive sulfur cycle from soda lakes. Extremophiles 12:431-439. http://dx.doi.org/10.1007/s00792-008-0148-8.
59. Hagerhall C, Hederstedt L. 1996. A structural model for the membraneintegral domain of succinate:quinone oxidoreductases. FEBS Lett 389:25-31. http://dx.doi.org/10.1016/0014-5793(96)00529-7.
60. Lin H, Hurt R, Jr, Johs A, Parks JM, Morrell-Falvey JL, Liang L, Elias D, Gu B. 2014. Unexpected effects of gene deletion on mercury interactions with the methylation-deficient mutant ΔhgcAB. Environ Sci Technol Lett 1:271-276. http://dx.doi.org/10.1021/ez500107r.
61. Thomsen MC, Nielsen M. 2012. Seq2Logo: a method for construction and visualization of amino acid binding motifs and sequence profiles including sequence weighting, pseudo counts and two-sided representation of amino acid enrichment and depletion. Nucleic Acids Res 40:W281-W287. http://dx.doi.org/10.1093/nar/gks469.