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Structure and function of the lanthanide-dependent methanol dehydrogenase XoxF from the methanotroph Methylomicrobium buryatense 5GB1C

Abstract

In methylotrophic bacteria, which use one-carbon (C1) compounds as a carbon source, methanol is oxidized by pyrroloquinoline quinone (PQQ)-dependent methanol dehydrogenase (MDH) enzymes. Methylotrophic genomes generally encode two distinct MDHs, MxaF and XoxF. MxaF is a well-studied, calcium-dependent heterotetrameric enzyme whereas XoxF is a lanthanide-dependent homodimer. Recent studies suggest that XoxFs are likely the functional MDHs in many environments. In methanotrophs, methylotrophs that utilize methane, interactions between particulate methane monooxygenase (pMMO) and MxaF have been detected. To investigate the possibility of interactions between pMMO and XoxF, XoxF was isolated from the methanotroph Methylomicrobium buryatense 5GB1C (5G-XoxF). Purified 5G-XoxF exhibits a specific activity of 0.16 μmol DCPIP reduced min−1 mg−1. The 1.85 Å resolution crystal structure reveals a La(III) ion in the active site, in contrast to the calcium ion in MxaF. The overall fold is similar to other MDH structures, but 5G-XoxF is a monomer in solution. An interaction between 5G-XoxF and its cognate pMMO was detected by biolayer interferometry, with a KD value of 50 ± 17 μM. These results suggest an alternative model of MDH-pMMO association, in which a XoxF monomer may bind to pMMO, and underscore the potential importance of lanthanide-dependent MDHs in biological methane oxidation.

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Abbreviations

ICP-MS:

Inductively coupled plasma mass spectrometry

ICP-OES:

Inductively coupled plasma optical emission spectrometry

Mc.:

Methylococcus

MDH:

Methanol dehydrogenase

Mm.:

Methylomicrobium

MMO:

Methane monooxygenase

pMMO:

Particulate methane monooxygenase

PQQ:

Pyrroloquinoline quinone

REE:

Rare earth element

SEC-MALS:

Size exclusion chromatography with multi-angle light scattering

References

  1. 1.

    Chistoserdova L, Kalyuzhnaya MG (2018) Trends Microbiol. 26:703–714. https://doi.org/10.1016/j.tim.2018.01.011

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Chistoserdova L, Lidstrom ME (2013) In: Rosenberg E, DeLong EF, Lory S, Stakebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin Heidelberg, pp 267–285

    Chapter  Google Scholar 

  3. 3.

    Strong PJ, Xie S, Clarke WP (2015) Environ Sci Technol 49:4001–4018

    CAS  Article  Google Scholar 

  4. 4.

    Pfeifenschneider J, Brautaset T, Wendisch VF (2017) Biofuels Bioprod Bioref 11:719–731

    CAS  Article  Google Scholar 

  5. 5.

    Keltjens JT, Pol A, Reimann J (2014) Op den Camp HJM. Appl Microbiol Biotechnol 98:6163–6183

    CAS  Article  Google Scholar 

  6. 6.

    Anthony C, Williams P (2003) Biochim Biophys Acta 1647:18–23

    CAS  Article  Google Scholar 

  7. 7.

    Skovran E, Martinez-Gomez NC (2015) Science 348:862–863

    CAS  Article  Google Scholar 

  8. 8.

    Chistoserdova L (2011) Environ Microbiol 13:2603–2622

    CAS  Article  Google Scholar 

  9. 9.

    Hibi Y, Asai K, Arafuka H, Hamajima M, Iwama T, Kawai K (2011) J Biosci Bioeng 111:547–549

    CAS  Article  Google Scholar 

  10. 10.

    Fitriyanto NA, Fushimi M, Matsunaga M, Pertiwiningrum A, Iwama T, Kawai K (2011) J Biosci Bioeng 111:613–617

    CAS  Article  Google Scholar 

  11. 11.

    Nakagawa T, Mitsui R, Tani A, Sasa K, Tashiro S, Iwama T, Hayakawa T, Kawai K (2012) PLoS One 7:e50480

    CAS  Article  Google Scholar 

  12. 12.

    Pol A, Barends TRM, Dietl A, Khadem AF, Eygensteyn J, Jetten MSM (2014) Op den Camp HJM. Environ Microbiol 16:255–264

    CAS  Article  Google Scholar 

  13. 13.

    Masuda S, Suzuki Y, Fujitani Y, Mitsui R, Nakagawa T, Shintani M, Tani A (2018) mSphere 3:e00462–17

    Article  Google Scholar 

  14. 14.

    Haque MFU, Kalidass B, Bandow N, Turpin EA, DiSpirito AA, Semrau JD (2015) Appl Environ Microbiol 81:7546–7552

    Article  Google Scholar 

  15. 15.

    Chu F, Lidstrom ME (2016) J Bacteriol 198:1317–1325

    CAS  Article  Google Scholar 

  16. 16.

    Vu HN, Subuyuj GA, Vijayakumar S, Good NM, Martinez-Gomez NC, Skovran E (2016) J Bacteriol 198:1250–1259

    CAS  Article  Google Scholar 

  17. 17.

    Bentlin FRS, Pozebon D (2010) J Braz Chem Soc 21:627–634

    CAS  Article  Google Scholar 

  18. 18.

    Jahn B, Pol A, Lumpe H, Barends TRM, Dietl A, Hogendoorn C, Op den Camp HJM, Daumann LJ (2018) ChemBioChem 19:1–8

    Article  Google Scholar 

  19. 19.

    Hanson RE, Hanson TE (1996) Microbiol Rev 60:439–471

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Sirajuddin S, Rosenzweig AC (2015) Biochemistry 54:2283–2294

    CAS  Article  Google Scholar 

  21. 21.

    Wadzinski AM, Ribbons DW (1975) J Bacteriol 122:1364–1374

    CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Fassel TA, Buchholz LA, Collins MLP, Remsen CC (1992) Appl Environ Microbiol 58:2302–2307

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Brantner C, Remsen C, Owen H, Buchholz L, Collins M (2002) Arch Microbiol 178:59–64

    CAS  Article  Google Scholar 

  24. 24.

    Kitmitto A, Myronova N, Basu P, Dalton H (2005) Biochemistry 44:10954–10965

    CAS  Article  Google Scholar 

  25. 25.

    Puri AW, Owen S, Chu F, Chavkin T, Beck DAC, Kalyuzhnaya MG, Lidstrom ME (2015) Appl Environ Microbiol 81:1775–1781

    Article  Google Scholar 

  26. 26.

    Culpepper MA, Rosenzweig AC (2014) Biochemistry 53:6211–6219

    CAS  Article  Google Scholar 

  27. 27.

    Myronova N, Kitmitto A, Collins RF, Miyaji A, Dalton H (2006) Biochemistry 45:11905–11914

    CAS  Article  Google Scholar 

  28. 28.

    de la Torre A, Metivier A, Chu F, Laurens LML, Beck DAC, Pienkos PT, Lidstrom ME, Kalyuzhnaya MG (2015) Microb Cell Fact 14:1–15

    Article  Google Scholar 

  29. 29.

    Choi D-W, Kunz RC, Boyd ES, Semrau JD, Antholine WE, Han JI, Zahn JA, Boyd JM, de la Mora AM, DiSpirito AA (2003) J Bacteriol 185:5755–5764

    CAS  Article  Google Scholar 

  30. 30.

    Day DJ, Anthony C (1990) Methods Enzymol 188:210–216

    CAS  Article  Google Scholar 

  31. 31.

    Ro SY, Ross MO, Deng Y, Batelu S, Lawton TJ, Hurley JD, Stemmler TL, Hoffman BM, Rosenzweig AC (2018) J Biol Chem 293:10457–10465. https://doi.org/10.1074/jbc.RA118.003348

    Article  PubMed  Google Scholar 

  32. 32.

    Otwinowski Z, Minor W (1997) Methods Enzymol 276:1–20

    Google Scholar 

  33. 33.

    McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) J Appl Cryst 40:658–674

    CAS  Article  Google Scholar 

  34. 34.

    Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Acta Crystallogr Sect D Biol Crystallogr 66:486–501

    CAS  Article  Google Scholar 

  35. 35.

    Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) Acta Crystallogr Sect D Biol Crystallogr 66:213–221

    CAS  Article  Google Scholar 

  36. 36.

    Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2009) Acta Crystallogr Sect D Biol Crystallogr 66:12–21

    Article  Google Scholar 

  37. 37.

    Laskowski RA (2000) Nucleic Acids Res 29:221–222

    Article  Google Scholar 

  38. 38.

    Wu ML, Wessels HJCT, Pol A, Op den Camp HJM, Jetten MSM, van Niftrik L, Keltjens JT (2015) Appl Environ Microbiol 81:1442–1451

    Article  Google Scholar 

  39. 39.

    Schmidt S, Christen P, Kiefer P, Vorholt JA (2010) Microbiology 156:2575–2586

    CAS  Article  Google Scholar 

  40. 40.

    Basu P, Katterle B, Andersson KK, Dalton H (2003) Biochem J 369:417–427

    CAS  Article  Google Scholar 

  41. 41.

    Anthony C (2004) Arch Biochem Biophys 428:2–9

    CAS  Article  Google Scholar 

  42. 42.

    Nojiri M, Hira D, Yamaguchi K, Okajima T, Tanizawa K, Suzuki S (2006) Biochemistry 45:3481–3492

    CAS  Article  Google Scholar 

  43. 43.

    Chan HTC, Anthony C (1991) Biochem J 280:139–146

    CAS  Article  Google Scholar 

  44. 44.

    Cox JM, Day DJ, Anthony C (1992) Biochim Biophys Acta 1119:97–106

    CAS  Article  Google Scholar 

  45. 45.

    Van Spanning RJM, Wansell CW, De Boer T, Hazelaar MJ, Anazawa H, Harms N, Oltmann LF, Stouthamer AH (1991) J Bacteriol 173:6948–6961

    Article  Google Scholar 

  46. 46.

    Anthony C (1992) Biochim Biophys Acta 1099:1–15

    CAS  Article  Google Scholar 

  47. 47.

    Choi JM, Cao T-P, Kim SW, Lee KH, Lee SH (2017) Proteins Struct Funct Bioinf 85:1379–1386

    CAS  Article  Google Scholar 

  48. 48.

    Skovran E, Palmer AD, Rountree AM, Good NM, Lidstrom ME (2011) J Bacteriol 193:6032–6038

    CAS  Article  Google Scholar 

  49. 49.

    Page MD, Anthony C (1986) J Gen Microb 132:1553–1563

    CAS  Google Scholar 

  50. 50.

    Goodwin MG, Anthony C (1996) Biochem J 318:673–679

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by NIH Grant GM118035 (A.C.R.) and a grant from the Undergraduate Research Grant Program which is administered by Northwestern University’s Office of Undergraduate Research. The authors thank Dr. Mary Lidstrom at Washington University for providing Mm. buryatense 5GB1C cultures and Theint Aung from the Northwestern Keck Biophysics Facility for assistance with BLItz instrumentation, data collection, and data interpretation. This work used the Advanced Photon Source, a US Department of Energy (DOE) Office of Science User Facility operated for the DOE Office of Science by Argonne National Laboratory under Contract No. DE-AC02-06CH11357. Use of the LS-CAT Sector 21 was supported by the Michigan Economic Development Corporation and the Michigan Technology Tri-Corridor (Grant 085P1000817). Data were collected at the LS-CAT beamlines 21-ID-D/F/G. Use of GM/CA has been funded in whole or in part with Federal funds from the National Cancer Institute (ACB-12002) and the National Institute of General Medical Sciences (AGM-12006). The GM/CA Eiger 16 M detector at beamline 23ID-B was funded by an NIH-Office of Research Infrastructure Programs, High-End Instrumentation Grant (1S10OD012289-01A1).

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Correspondence to Amy C. Rosenzweig.

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PDB accession code: 6DAM.

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Deng, Y.W., Ro, S.Y. & Rosenzweig, A.C. Structure and function of the lanthanide-dependent methanol dehydrogenase XoxF from the methanotroph Methylomicrobium buryatense 5GB1C. J Biol Inorg Chem 23, 1037–1047 (2018). https://doi.org/10.1007/s00775-018-1604-2

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Keywords

  • Lanthanide
  • Methanol dehydrogenase
  • Methanotroph
  • XoxF
  • Particulate methane monooxygenase