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Multi-omics reveal various potential antimonate reductases from phylogenetically diverse microorganisms

  • Ling-Dong Shi
  • Min Wang
  • Yu-Lin Han
  • Chun-Yu Lai
  • James P. Shapleigh
  • He-Ping ZhaoEmail author
Environmental biotechnology

Abstract

While previous work has demonstrated that antimonate (Sb(V)) can be bio-reduced with methane as the sole electron donor, the microorganisms responsible for Sb(V) reduction remain largely uncharacterized. Inspired by the recently reported Sb(V) reductase belonging to the dimethyl sulfoxide reductase (DMSOR) family, this study was undertaken to use metagenomics and metatranscriptomics to unravel whether any DMSOR family genes in the bioreactor had the potential for Sb(V) reduction. A search through metagenomic-assembled genomes recovered from the microbial community found that some DMSOR family genes, designated sbrA (Sb(V) reductase gene), were highly transcribed in four phylogenetically disparate assemblies. The putative catalytic subunits were found to be representatives of two distinct phylogenetic clades of reductases that were most closely related to periplasmic nitrate reductases and respiratory arsenate reductases, respectively. Putative operons containing sbrA possessed many other components, including genes encoding c-type cytochromes, response regulators, and ferredoxins, which together implement Sb(V) reduction. This predicted ability was confirmed by incubating the enrichment culture with 13C-labeled CH4 and Sb(V) in serum bottles, where Sb(V) was reduced coincident with the production of 13C-labeled CO2. Overall, these results increase our understanding of how Sb(V) can be bio-reduced in environments.

Keywords

Antimonate reduction Molybdenum-containing Dimethyl sulfoxide reductase family Methane oxidation 

Notes

Funding information

The authors received financial support from the “National Key Technology R&D Program (2018YFC1802203),” the “National Natural Science Foundation of China (Grant No. 51878596, 21577123),” and the “Natural Science Funds for Distinguished Young Scholar of Zhejiang Province (LR17B070001).”

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

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References

  1. Abin CA, Hollibaugh JT (2014) Dissimilatory antimonate reduction and production of antimony trioxide microcrystals by a novel microorganism. Environ Sci Technol 48(1):681–688.  https://doi.org/10.1021/es404098z CrossRefGoogle Scholar
  2. Abin CA, Hollibaugh JT (2019) Transcriptional response of the obligate anaerobe Desulfuribacillus stibiiarsenatis MLFW-2(T) to growth on antimonate and other terminal electron acceptors. Environ Microbiol 21(2):618–630.  https://doi.org/10.1111/1462-2920.14503 Google Scholar
  3. Agency USEP (2015) Appendix A to Subpart O - Regulated Contaminants.Google Scholar
  4. Anderson GL, Williams J, Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem 267(33):23674–23682Google Scholar
  5. Arkin AP, Cottingham RW, Henry CS, Harris NL, Stevens RL, Maslov S, Dehal P, Ware D, Perez F, Canon S, Sneddon MW, Henderson ML, Riehl WJ, Murphy-Olson D, Chan SY, Kamimura RT, Kumari S, Drake MM, Brettin TS, Glass EM, Chivian D, Gunter D, Weston DJ, Allen BH, Baumohl J, Best AA, Bowen B, Brenner SE, Bun CC, Chandonia JM, Chia JM, Colasanti R, Conrad N, Davis JJ, Davison BH, DeJongh M, Devoid S, Dietrich E, Dubchak I, Edirisinghe JN, Fang G, Faria JP, Frybarger PM, Gerlach W, Gerstein M, Greiner A, Gurtowski J, Haun HL, He F, Jain R, Joachimiak MP, Keegan KP, Kondo S, Kumar V, Land ML, Meyer F, Mills M, Novichkov PS, Oh T, Olsen GJ, Olson R, Parrello B, Pasternak S, Pearson E, Poon SS, Price GA, Ramakrishnan S, Ranjan P, Ronald PC, Schatz MC, Seaver SMD, Shukla M, Sutormin RA, Syed MH, Thomason J, Tintle NL, Wang DF, Xia FF, Yoo H, Yoo S, Yu DT (2018) KBase: The United States Department of Energy Systems Biology Knowledgebase. Nat Biotechnol 36(7):566–569.  https://doi.org/10.1038/Nbt.4163 CrossRefGoogle Scholar
  6. Arnoux P, Sabaty M, Alric J, Frangioni B, Guigliarelli B, Adriano JM, Pignol D (2003) Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase. Nat Struct Biol 10(11):928–934.  https://doi.org/10.1038/nsb994 CrossRefGoogle Scholar
  7. Bar-Or I, Elvert M, Eckert W, Kushmaro A, Vigderovich H, Zhu Q, Ben-Dov E, Sivan O (2017) Iron-coupled anaerobic oxidation of methane performed by a mixed bacterial-archaeal community based on poorly reactive minerals. Environ Sci Technol.  https://doi.org/10.1021/acs.est.7b03126
  8. Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD (1997) Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. Science 275(5304):1305–1308.  https://doi.org/10.1126/science.275.5304.1305 CrossRefGoogle Scholar
  9. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA, Stevens R, Vonstein V, Wattam AR, Xia FF (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365.  https://doi.org/10.1038/Srep08365
  10. Bursakov SA, Carneiro C, Almendra MJ, Duarte RO, Caldeira J, Moura I, Moura JJG (1997) Enzymatic properties and effect of ionic strength on periplasmic nitrate reductase (NAP) from Desulfovibrio desulfuricans ATCC 27774. Biochem Biophys Res Commun 239(3):816–822.  https://doi.org/10.1006/bbrc.1997.7560 CrossRefGoogle Scholar
  11. Chen R, Luo YH, Chen JX, Zhang Y, Wen LL, Shi LD, Tang YN, Rittmann BE, Zheng P, Zhao HP (2016) Evolution of the microbial community of the biofilm in a methane-based membrane biofilm reactor reducing multiple electron acceptors. Environ Sci Pollut Res 23(10):9540–9548.  https://doi.org/10.1007/s11356-016-6146-y CrossRefGoogle Scholar
  12. Costa C, Dijkema C, Friedrich M, Garcia-Encina P, Fernandez-Polanco F, Stams AJM (2000) Denitrification with methane as electron donor in oxygen-limited bioreactors. Appl Microbiol Biotechnol 53(6):754–762.  https://doi.org/10.1007/s002530000337 CrossRefGoogle Scholar
  13. Danilova OV, Suzina NE, Van De Kamp J, Svenning MM, Bodrossy L, Dedysh SN (2016) A new cell morphotype among methane oxidizers: a spiral-shaped obligately microaerophilic methanotroph from northern low-oxygen environments. Isme J 10(11):2734–2743.  https://doi.org/10.1038/ismej.2016.48 CrossRefGoogle Scholar
  14. Department of Environmental Protection JP, China (2018) Discharge standard of antimony pollutants in wasterwater for textile dyeing and finishing. DB 32/3432-2018Google Scholar
  15. Filella M, Belzile N, Chen YW (2002) Antimony in the environment: a review focused on natural waters I. Occurrence. Earth Sci Rev 57(1-2):125–176.  https://doi.org/10.1016/S0012-8252(01)00070-8 CrossRefGoogle Scholar
  16. Grimaldi S, Schoepp-Cothenet B, Ceccaldi P, Guigliarelli B, Magalon A (2013) The prokaryotic Mo/W-bisPGD enzymes family: a catalytic workhorse in bioenergetic. Bba-Bioenergetics 1827(8-9):1048–1085.  https://doi.org/10.1016/j.bbabio.2013.01.011 CrossRefGoogle Scholar
  17. Jepson BJN, Mohan S, Clarke TA, Gates AJ, Cole JA, Butler CS, Butt JN, Hemmings AM, Richardson DJ (2007) Spectropotentiometric and structural analysis of the periplasmic nitrate reductase from Escherichia coli. J Biol Chem 282(9):6425–6437.  https://doi.org/10.1074/jbc.M607353200 CrossRefGoogle Scholar
  18. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG Tools for functional characterization of genome and metagenome sequences. J Mol Biol 428(4):726–731.  https://doi.org/10.1016/j.jmb.2015.11.006 CrossRefGoogle Scholar
  19. Kang DWD, Froula J, Egan R, Wang Z (2015) MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. Peerj 3:e1165.  https://doi.org/10.7717/Peerj.1165
  20. Kengen SWM, Rikken GB, Hagen WR, van Ginkel CG, Stams AJM (1999) Purification and characterization of (per)chlorate reductase from the chlorate-respiring strain GR-1. J Bacteriol 181(21):6706–6711Google Scholar
  21. Kits KD, Klotz MG, Stein LY (2015) Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp nov type strain FJG1. Environ Microbiol 17(9):3219–3232.  https://doi.org/10.1111/1462-2920.12772 CrossRefGoogle Scholar
  22. Krafft T, Macy JM (1998) Purification and characterization of the respiratory arsenate reductase of Chrysiogenes arsenatis. Eur J Biochem 255(3):647–653.  https://doi.org/10.1046/j.1432-1327.1998.2550647.x CrossRefGoogle Scholar
  23. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580.  https://doi.org/10.1006/jmbi.2000.4315 CrossRefGoogle Scholar
  24. Kulp TR, Miller LG, Braiotta F, Webb SM, Kocar BD, Blum JS, Oremland RS (2014) Microbiological reduction of Sb(V) in anoxic freshwater sediments. Environ Sci Technol 48(1):218–226.  https://doi.org/10.1021/es403312j CrossRefGoogle Scholar
  25. Lai CY, Wen LL, Zhang Y, Luo SS, Wang QY, Luo YH, Chen R, Yang X, Rittmann BE, Zhao HP (2016) Autotrophic antimonate bio-reduction using hydrogen as the electron donor. Water Res 88:467–474.  https://doi.org/10.1016/j.watres.2015.10.042 CrossRefGoogle Scholar
  26. Lai CY, Dong QY, Rittmann BE, Zhao HP (2018) Bioreduction of antimonate by anaerobic methane oxidation in a membrane biofilm batch reactor. Environ Sci Technol 52(15):8693–8700.  https://doi.org/10.1021/acs.est.8b02035 CrossRefGoogle Scholar
  27. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–U54.  https://doi.org/10.1038/Nmeth.1923 CrossRefGoogle Scholar
  28. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefGoogle Scholar
  29. Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, Yamashita H, Lam TW (2016) MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102:3–11.  https://doi.org/10.1016/j.ymeth.2016.02.020 CrossRefGoogle Scholar
  30. Liu FY, Le XC, McKnight-Whitford A, Xia YL, Wu FC, Elswick E, Johnson CC, Zhu C (2010) Antimony speciation and contamination of waters in the Xikuangshan antimony mining and smelting area, China. Environ Geochem Health 32(5):401–413.  https://doi.org/10.1007/s10653-010-9284-z CrossRefGoogle Scholar
  31. Luo YH, Chen R, Wen LL, Meng F, Zhang Y, Lai CY, Rittmann BE, Zhao HP, Zheng P (2015) Complete perchlorate reduction using methane as the sole electron donor and carbon source. Environ Sci Technol 49(4):2341–2349.  https://doi.org/10.1021/es504990m CrossRefGoogle Scholar
  32. Lv PL, Shi LD, Wang Z, Rittmann BE, Zhao HP (2019) Methane oxidation coupled to perchlorate reduction in a membrane biofilm batch reactor. Sci Total Environ 667:9–15.  https://doi.org/10.1016/j.scitotenv.2019.02.330 CrossRefGoogle Scholar
  33. Martinez-Cruz K, Leewis MC, Herriott IC, Sepulveda-Jauregui A, Anthony KW, Thalasso F, Leigh MB (2017) Anaerobic oxidation of methane by aerobic methanotrophs in sub-Arctic lake sediments. Sci Total Environ 607:23–31.  https://doi.org/10.1016/j.scitotenv.2017.06.187 CrossRefGoogle Scholar
  34. Masscheleyn PH, Delaune RD, Patrick WH (1991) Effect of redox potential and Ph on arsenic speciation and solubility in a contaminated soil. Environ Sci Technol 25(8):1414–1419.  https://doi.org/10.1021/Es00020a008 CrossRefGoogle Scholar
  35. McEwan AG, Ridge JP, McDevitt CA, Hugenholtz P (2002) The DMSO reductase family of microbial molybdenum enzymes; molecular properties and role in the dissimilatory reduction of toxic elements. Geomicrobiol J 19(1):3–21.  https://doi.org/10.1080/014904502317246138 CrossRefGoogle Scholar
  36. Moreno-Vivian C, Cabello P, Martinez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181(21):6573–6584Google Scholar
  37. Naqvi SWA, Lam P, Narvenkar G, Sarkar A, Naik H, Pratihary A, Shenoy DM, Gauns M, Kurian S, Damare S, Duret M, Lavik G, Kuypers MMM (2018) Methane stimulates massive nitrogen loss from freshwater reservoirs in India. Nat Commun 9.  https://doi.org/10.1038/S41467-018-03607-Z
  38. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25(7):1043–1055.  https://doi.org/10.1101/gr.186072.114 CrossRefGoogle Scholar
  39. Pertea M, Pertea GM, Antonescu CM, Chang TC, Mendell JT, Salzberg SL (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol 33(3):290–29+.  https://doi.org/10.1038/nbt.3122 CrossRefGoogle Scholar
  40. Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46(W1):W200–W204.  https://doi.org/10.1093/nar/gky448 CrossRefGoogle Scholar
  41. Rodriguez-R LM, Gunturu S, Harvey WT, Rossello-Mora R, Tiedje JM, Cole JR, Konstantinidis KT (2018) The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res 46(W1):W282–W288.  https://doi.org/10.1093/nar/gky467 CrossRefGoogle Scholar
  42. Schroder I, Rech S, Krafft T, Macy JM (1997) Purification and characterization of the selenate reductase from Thauera selenatis. J Biol Chem 272(38):23765–23768.  https://doi.org/10.1074/jbc.272.38.23765 CrossRefGoogle Scholar
  43. Song SH, Yeom SH, Choi SS, Yoo YJ (2003) Effect of oxidation-reduction potential on denitrification by Ochrobactrum anthropi SY509. J Microbiol Biotechnol 13(3):473–476Google Scholar
  44. Sundar S, Chakravarty J (2010) Antimony toxicity. Int J Environ Res Public Health 7(12):4267–4277.  https://doi.org/10.3390/ijerph7124267 CrossRefGoogle Scholar
  45. Sundermeyerklinger H, Meyer W, Warninghoff B, Bock E (1984) Membrane-bound nitrite oxidoreductase of Nitrobacter: evidence for a nitrate reductase system. Arch Microbiol 140(2-3):153–158.  https://doi.org/10.1007/Bf00454918 CrossRefGoogle Scholar
  46. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefGoogle Scholar
  47. Wang Q, Warelow TP, Kang YS, Romano C, Osborne TH, Lehr CR, Bothner B, McDermott TR, Santini JM, Wang GJ (2015) Arsenite oxidase also functions as an antimonite oxidase. Appl Environ Microbiol 81(6):1959–1965.  https://doi.org/10.1128/Aem.02981-14 CrossRefGoogle Scholar
  48. Wang NN, Wang AH, Kong LH, He MC (2018) Calculation and application of Sb toxicity coefficient for potential ecological risk assessment. Sci Total Environ 610:167–174.  https://doi.org/10.1016/j.scitotenv.2017.07.268 CrossRefGoogle Scholar
  49. Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins 64(3):643–651.  https://doi.org/10.1002/prot.21018 CrossRefGoogle Scholar
  50. Zhao HP, Van Ginkel S, Tang Y, Kang DW, Rittmann B, Krajmalnik-Brown R (2011) Interactions between perchlorate and nitrate reductions in the biofilm of a hydrogen-based membrane biofilm reactor. Environ Sci Technol 45(23):10155–10162.  https://doi.org/10.1021/es202569b CrossRefGoogle Scholar
  51. Zhu J, Wang Q, Yuan MD, Tan GYA, Sun FQ, Wang C, Wu WX, Lee PH (2016) Microbiology and potential applications of aerobic methane oxidation coupled to denitrification (AME-D) process: a review. Water Res 90:203–215.  https://doi.org/10.1016/j.watres.2015.12.020 CrossRefGoogle Scholar
  52. Zotov AV, Shikina ND, Akinfiev NN (2003) Thermodynamic properties of the Sb(III) hydroxide complex Sb(OH)(3(aq)) at hydrothermal conditions. Geochim Cosmochim Acta 67(10):1821–1836.  https://doi.org/10.1016/S0016-7037(00)01281-4 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.MOE Key Lab of Environmental Remediation and Ecosystem Health, College of Environmental and Resource ScienceZhejiang UniversityHangzhouChina
  2. 2.Zhejiang Prov Key Lab Water Pollut Control & EnviZhejiang UniversityZhejiangChina
  3. 3.Advanced Water Management CentreThe University of QueenslandSt. LuciaAustralia
  4. 4.Department of MicrobiologyCornell UniversityIthacaUSA

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