1887

Abstract

The sulfate-reducing, mercury-methylating strain ND132 was isolated from the brackish anaerobic bottom sediments of Chesapeake Bay, USA. Capable of high levels of mercury (Hg) methylation, ND132 has been widely used as a model strain to study the process and to determine the genetic basis of Hg methylation. Originally called ND132 on the basis of an early partial 16S rRNA sequence, the strain has never been formally described. Phylogenetic and physiological traits place this strain within the genus in the recently reclassified phylum (formerly ). ND132 is most closely related to BerOc1 and J2. Analysis of average nucleotide identity (ANI) of whole-genome sequences showed roughly 88 % ANI between BerOc1 and ND132, and 84 % similarity between ND132 and J2. These cut-off scores <95 %, along with a multi-gene phylogenetic analysis of members of the family and differences in physiology indicate that all three strains represent separate species. The Gram-stain-negative cells are vibrio-shaped, motile and not sporulated. ND132 is a salt-tolerant mesophile with optimal growth in the laboratory at 32 °C, 2 % salinity, and pH 7.8. The DNA G+C content of the genomic DNA is 65.2 %. It is an incomplete oxidizer of short chain fatty acids, using lactate, pyruvate and fumarate with sulfate or sulfite as the terminal electron acceptors. ND132 can respire fumarate using pyruvate as an electron donor. The major fatty acids are iso-C, anteiso-C, iso-C, iso-Cω9 and anteiso-C. We propose the classification of strain ND132 (DSM 110689, ATCC TSD-224) as the type strain sp. nov.

Funding
This study was supported by the:
  • DwayneA Elias , Oak Ridge National Laboratory (US)
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.004697
2021-02-11
2021-02-26
Loading full text...

Full text loading...

References

  1. Benoit JM, Gilmour CC, Mason RP. The influence of sulfide on solid-phase mercury bioavailability for methylation by pure cultures of Desulfobulbus propionicus (1pr3). Environ Sci Technol 2001; 35: 127 132 [CrossRef] [PubMed]
    [Google Scholar]
  2. Benoit JM, Gilmour CC, Mason RP. Aspects of bioavailability of mercury for methylation in pure cultures of Desulfobulbus propionicus (1pr3). Appl Environ Microbiol 2001; 67: 51 58 [CrossRef] [PubMed]
    [Google Scholar]
  3. Jay JA, Murray KJ, Gilmour CC, Mason RP, Morel FMM et al. Mercury methylation by Desulfovibrio desulfuricans ND132 in the presence of polysulfides. Appl Environ Microbiol 2002; 68: 5741 5745 [CrossRef] [PubMed]
    [Google Scholar]
  4. Lu X, Johs A, Zhao L, Wang L, Pierce EM et al. Nanomolar copper enhances mercury methylation by Desulfovibrio desulfuricans ND132. Environ Sci Technol Lett 2018; 5: 372 376 [CrossRef]
    [Google Scholar]
  5. Graham AM, Cameron-Burr KT, Hajic HA, Lee C, Msekela D et al. Sulfurization of dissolved organic matter increases Hg-sulfide-dissolved organic matter bioavailability to a Hg-methylating bacterium. Environ Sci Technol 2017; 51: 9080 9088 [CrossRef] [PubMed]
    [Google Scholar]
  6. Graham AM, Bullock AL, Maizel AC, Elias DA, Gilmour CC. Detailed assessment of the kinetics of Hg-cell association, Hg methylation, and methylmercury degradation in several Desulfovibrio species. Appl Environ Microbiol 2012; 78: 7337 7346 [CrossRef] [PubMed]
    [Google Scholar]
  7. Graham AM, Aiken GR, Gilmour CC. Dissolved organic matter enhances microbial mercury methylation under sulfidic conditions. Environ Sci Technol 2012; 46: 2715 2723 [CrossRef] [PubMed]
    [Google Scholar]
  8. An J, Zhang L, Lu X, Pelletier DA, Pierce EM et al. Mercury uptake by Desulfovibrio desulfuricans ND132: passive or active?. Environ Sci Technol 2019; 53: 6264 6272 [CrossRef] [PubMed]
    [Google Scholar]
  9. Zhao L, Chen H, Lu X, Lin H, Christensen GA et al. Contrasting effects of dissolved organic matter on mercury methylation by Geobacter sulfurreducens PCA and Desulfovibrio desulfuricans ND132. Environ Sci Technol 2017; 51: 10468 10475 [CrossRef] [PubMed]
    [Google Scholar]
  10. Liu Y-R, Lu X, Zhao L, An J, He J-Z et al. Effects of cellular sorption on mercury bioavailability and methylmercury production by Desulfovibrio desulfuricans ND132. Environ Sci Technol 2016; 50: 13335 13341 [CrossRef] [PubMed]
    [Google Scholar]
  11. Schaefer JK, Rocks SS, Zheng W, Liang L, Gu B et al. Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria. Proc Natl Acad Sci U S A 2011; 108: 8714 8719 [CrossRef]
    [Google Scholar]
  12. Rivera NA, Bippus PM, Hsu-Kim H. Relative reactivity and bioavailability of mercury sorbed to or coprecipitated with aged iron sulfides. Environ Sci Technol 2019; 53: 7391 7399 [CrossRef] [PubMed]
    [Google Scholar]
  13. Gilmour CC, Tuttle JH, Means JC. Anaerobic microbial methylation of inorganic tin in estuarine sediment slurries. Microb Ecol 1987; 14: 233 242 [CrossRef] [PubMed]
    [Google Scholar]
  14. Gilmour CC, Elias DA, Kucken AM, Brown SD, Palumbo AV et al. Sulfate-reducing bacterium Desulfovibrio desulfuricans ND132 as a model for understanding bacterial mercury methylation. Appl Environ Microbiol 2011; 77: 3938 3951 [CrossRef] [PubMed]
    [Google Scholar]
  15. Brown SD, Gilmour CC, Kucken AM, Wall JD, Elias DA. Genome sequence of the mercury-methylating strain Desulfovibrio desulfuricans ND132. J Bacteriol 2011; 193: 2078 2079 [CrossRef] [PubMed]
    [Google Scholar]
  16. Hurt RA, Brown SD, Podar M, Palumbo AV, Elias DA. Sequencing intractable DNA to close microbial genomes. PLoS One 2012; 7: e41295 [CrossRef] [PubMed]
    [Google Scholar]
  17. Gilmour C. Estuarine methylation of tin and its relationship to the microbial sulfur cycle. University of Maryland 1985
    [Google Scholar]
  18. Podar M, Gilmour CC, Brandt CC, Soren A, Brown SD et al. Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci Adv 2015; 1: e1500675 [CrossRef] [PubMed]
    [Google Scholar]
  19. Gilmour CC, Bullock AL, McBurney A, Podar M, Elias DA. Robust mercury methylation across diverse methanogenic Archaea . mBio 2018; 9: e02403 02417 [CrossRef] [PubMed]
    [Google Scholar]
  20. Parks JM, Johs A, Podar M, Bridou R, Hurt RA et al. The genetic basis for bacterial mercury methylation. Science 2013; 339: 1332 1335 [CrossRef] [PubMed]
    [Google Scholar]
  21. Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD et al. Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 2013; 47: 11810 11820 [CrossRef] [PubMed]
    [Google Scholar]
  22. Ranchou-Peyruse M, Monperrus M, Bridou R, Duran R, Amouroux D et al. Overview of mercury methylation capacities among anaerobic bacteria including representatives of the sulphate-reducers: implications for environmental studies. Geomicrobiol J 2009; 26: 1 8 [CrossRef]
    [Google Scholar]
  23. Goñi-Urriza M, Klopp C, Ranchou-Peyruse M, Ranchou-Peyruse A, Monperrus M. Genome insights of mercury methylation among Desulfovibrio and Pseudodesulfovibrio strains. Research in microbiology 2019
    [Google Scholar]
  24. Bowman KL, Collins RE, Agather AM, Lamborg CH, Hammerschmidt CR. Distribution of mercury‐cycling genes in the Arctic and equatorial Pacific Oceans and their relationship to mercury speciation. Limnology and Oceanography 2019
    [Google Scholar]
  25. Christensen GA, Gionfriddo CM, King AJ, Moberly JG, Miller CL et al. Determining the reliability of measuring mercury cycling gene abundance with correlations with mercury and methylmercury concentrations. Environ Sci Technol 2019; 53: 8649 8663 [CrossRef] [PubMed]
    [Google Scholar]
  26. Gionfriddo CM, Tate MT, Wick RR, Schultz MB, Zemla A et al. Microbial mercury methylation in Antarctic sea ice. Nat Microbiol 2016; 1: 16127 [CrossRef] [PubMed]
    [Google Scholar]
  27. Jones DS, Walker GM, Johnson NW, Mitchell CPJ, Coleman Wasik JK et al. Molecular evidence for novel mercury methylating microorganisms in sulfate-impacted lakes. Isme J 2019; 13: 1659 1675 [CrossRef] [PubMed]
    [Google Scholar]
  28. Gionfriddo CM, e al. Expanded Hg-methylator diversity in nature, using an improved hgcAB primer set and direct high-throughput sequencing. In Review 2020
    [Google Scholar]
  29. Colombo MJ, Ha J, Reinfelder JR, Barkay T, Yee N. Anaerobic oxidation of Hg(0) and methylmercury formation by Desulfovibrio desulfuricans ND132. Geochim Cosmochim Acta 2013; 112: 166 177 [CrossRef]
    [Google Scholar]
  30. Hu H, Lin H, Zheng W, Tomanicek SJ, Johs A et al. Oxidation and methylation of dissolved elemental mercury by anaerobic bacteria. Nat Geosci 2013; 6: 751 754 [CrossRef]
    [Google Scholar]
  31. Wang Y, Schaefer JK, Mishra B, Yee N. Intracellular Hg(0) oxidation in Desulfovibrio desulfuricans ND132. Environ Sci Technol 2016; 50: 11049 11056 [CrossRef] [PubMed]
    [Google Scholar]
  32. Janssen SE, Schaefer JK, Barkay T, Reinfelder JR. Fractionation of mercury stable isotopes during microbial methylmercury production by iron- and sulfate-reducing bacteria. Environ Sci Technol 2016; 50: 8077 8083 [CrossRef] [PubMed]
    [Google Scholar]
  33. Gilmour CC, Leavitt ME, Shiaris MP. Evidence against incorporation of exogenous thymidine by sulfate-reducing bacteria. Limnol Oceanogr 1990; 35: 1401 1409 [CrossRef]
    [Google Scholar]
  34. Dolor MK, Gilmour CC, Helz GR. Distinct microbial behavior of Re compared to Tc: evidence against microbial Re fixation in aquatic sediments. Geomicrobiol J 2009; 26: 470 483 [CrossRef]
    [Google Scholar]
  35. Smith SD, Bridou R, Johs A, Parks JM, Elias DA et al. Site-directed mutagenesis of HgcA and HgcB reveals amino acid residues important for mercury methylation. Appl Environ Microbiol 2015; 81: 3205 3217 [CrossRef] [PubMed]
    [Google Scholar]
  36. Date SS, Parks JM, Rush KW, Wall JD, Ragsdale SW et al. Kinetics of enzymatic mercury methylation at nanomolar concentrations catalyzed by HgcAB. Appl Environ Microbiol 2019; 85: e00438 00419 [CrossRef] [PubMed]
    [Google Scholar]
  37. Cooper CJ, Zheng K, Rush KW, Johs A, Sanders BC et al. Structure determination of the HgcAB complex using metagenome sequence data: insights into microbial mercury methylation. Commun Biol 2020; 3: 1 9 [CrossRef]
    [Google Scholar]
  38. Campbell LL, Kasprzycki MA, Postgate JR, Ma PJR. Desulfovibrio africanus sp. nov - a new dissimilatory sulfate-reducing bacterium. J Bacteriol 1966; 92: 1122 1127 [CrossRef] [PubMed]
    [Google Scholar]
  39. Devereux R, He SH, Doyle CL, Orkland S, Stahl D et al. Diversity and origin of Desulfovibrio species: phylogenetic definition of a family. J Bacteriol 1990; 172: 3609 3619 [CrossRef] [PubMed]
    [Google Scholar]
  40. Cao J, Gayet N, Zeng X, Shao Z, Jebbar M et al. Pseudodesulfovibrio indicus gen. nov., sp. nov., a piezophilic sulfate-reducing bacterium from the Indian Ocean and reclassification of four species of the genus Desulfovibrio . Int J Syst Evol Microbiol 2016; 66: 3904 3911 [CrossRef] [PubMed]
    [Google Scholar]
  41. Sun B, Cole JR, Sanford RA, Tiedje JM. Isolation and characterization of Desulfovibrio dechloracetivorans sp. nov., a marine dechlorinating bacterium growing by coupling the oxidation of acetate to the reductive dechlorination of 2-chlorophenol. Appl Environ Microbiol 2000; 66: 2408 2413 [CrossRef] [PubMed]
    [Google Scholar]
  42. Ranchou-Peyruse M, Goñi-Urriza M, Guignard M, Goas M, Ranchou-Peyruse A et al. Pseudodesulfovibrio hydrargyri sp. nov., a mercury-methylating bacterium isolated from a brackish sediment. Int J Syst Evol Microbiol 2018; 68: 1461 1466 [CrossRef] [PubMed]
    [Google Scholar]
  43. Goñi-Urriza M, Klopp C, Ranchou-Peyruse M, Ranchou-Peyruse A, Monperrus M et al. Genome insights of mercury methylation among Desulfovibrio and Pseudodesulfovibrio strains. Res Microbiol 2020; 171: 3 12 [CrossRef] [PubMed]
    [Google Scholar]
  44. Waite DW, Chuvochina M, Pelikan C, Parks DH, Yilmaz P et al. Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol 2020; 70: 5972 6016 [CrossRef] [PubMed]
    [Google Scholar]
  45. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312 1313 [CrossRef] [PubMed]
    [Google Scholar]
  46. Kim YJ, Yang J-A, Lim JK, Park M-J, Yang S-H et al. Paradesulfovibrio onnuriensis gen. nov., sp. nov., a chemolithoautotrophic sulfate-reducing bacterium isolated from the Onnuri vent field of the Indian Ocean and reclassification of Desulfovibrio senegalensis as Paradesulfovibrio senegalensis comb. nov. J Microbiol 2020; 58: 252 259 [CrossRef] [PubMed]
    [Google Scholar]
  47. Thioye A, Gam ZBA, Mbengue M, Cayol J-L, Joseph-Bartoli M et al. Desulfovibrio senegalensis sp. nov., a mesophilic sulfate reducer isolated from marine sediment. Int J Syst Evol Microbiol 2017; 67: 3162 3166 [CrossRef] [PubMed]
    [Google Scholar]
  48. Miller LT. Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 1982; 16: 584 586 [CrossRef] [PubMed]
    [Google Scholar]
  49. Kuykendall L, Roy M, O'neill J, Devine T. Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum . Int J Syst Evol Microbiol 1988; 38: 358 361
    [Google Scholar]
  50. Taylor J, Parkes RJ. The cellular fatty acids of the sulphate-reducing bacteria, Desulfobacter sp., Desulfobulbus sp. and Desulfovibrio desulfuricans . Microbiology 1983; 129: 3303 3309 [CrossRef]
    [Google Scholar]
  51. Edlund A, Nichols PD, Roffey R, White DC. Extractable and lipopolysaccharide fatty acid and hydroxy acid profiles from Desulfovibrio species. J Lipid Res 1985; 26: 982 988 [CrossRef] [PubMed]
    [Google Scholar]
  52. Choi SC, Chase T, Bartha R. Enzymatic catalysis of mercury methylation by Desulfovibrio desulfuricans LS. Appl Environ Microbiol 1994; 60: 1342 1346 [CrossRef] [PubMed]
    [Google Scholar]
  53. Choi SC, Bartha R. Cobalamin-mediated mercury methylation by Desulfovibrio desulfuricans LS. Appl Environ Microbiol 1993; 59: 290 295 [CrossRef] [PubMed]
    [Google Scholar]
  54. Suzuki D, Ueki A, Amaishi A, Ueki K. Desulfovibrio portus sp. nov., a novel sulfate-reducing bacterium in the class Deltaproteobacteria isolated from an estuarine sediment. J Gen Appl Microbiol 2009; 55: 125 133 [CrossRef] [PubMed]
    [Google Scholar]
  55. Khelaifia S, Fardeau M-L, Pradel N, Aussignargues C, Garel M et al. Desulfovibrio piezophilus sp. nov., a piezophilic, sulfate-reducing bacterium isolated from wood falls in the Mediterranean sea. Int J Syst Evol Microbiol 2011; 61: 2706 2711 [CrossRef] [PubMed]
    [Google Scholar]
  56. Bale SJ, Goodman K, Rochelle PA, Marchesi JR, Fry JC et al. Desulfovibrio profundus sp. nov., a novel barophilic sulfate-reducing bacterium from deep sediment layers in the Japan sea. Int J Syst Bacteriol 1997; 47: 515 521 [CrossRef] [PubMed]
    [Google Scholar]
  57. Motamedi M, Pedersen K. Desulfovibrio aespoeensis sp. nov., a mesophilic sulfate-reducing bacterium from deep groundwater at Aspö hard rock laboratory, Sweden. Int J Syst Bacteriol 1998; 48 Pt 1: 311 315 [CrossRef] [PubMed]
    [Google Scholar]
  58. Caumette P, Cohen Y, Matheron R. Isolation and characterization of Desulfovibrio halophilus sp. nov., a halophilic sulfate-reducing bacterium isolated from solar lake (Sinai). Syst Appl Microbiol 1991; 14: 33 38 [CrossRef]
    [Google Scholar]
  59. Krekeler D, Sigalevich P, Teske A, Cypionka H, Cohen Y. A sulfate-reducing bacterium from the oxic layer of a microbial mat from solar lake (Sinai), Desulfovibrio oxyclinae sp. nov. Arch Microbiol 1997; 167: 369 375 [CrossRef]
    [Google Scholar]
  60. Warthmann R, Vasconcelos C, Sass H, McKenzie JA. Desulfovibrio brasiliensis sp. nov., a moderate halophilic sulfate-reducing bacterium from Lagoa Vermelha (Brazil) mediating dolomite formation. Extremophiles 2005; 9: 255 261 [CrossRef] [PubMed]
    [Google Scholar]
  61. Ben Ali Gam Z, Oueslati R, Abdelkafi S, Casalot L, Tholozan JL et al. Desulfovibrio tunisiensis sp. nov., a novel weakly halotolerant, sulfate-reducing bacterium isolated from exhaust water of a Tunisian oil refinery. Int J Syst Evol Microbiol 2009; 59: 1059 1063 [CrossRef] [PubMed]
    [Google Scholar]
  62. Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD et al. Genbank. Nucleic Acids Res 2019; 47: D94 D99 [CrossRef] [PubMed]
    [Google Scholar]
  63. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25: 1043 1055 [CrossRef] [PubMed]
    [Google Scholar]
  64. Criscuolo A, Gribaldo S. BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010; 10: 210 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.004697
Loading
/content/journal/ijsem/10.1099/ijsem.0.004697
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error