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Extremophiles

, Volume 19, Issue 1, pp 109–118 | Cite as

Characterization of the frhAGB-encoding hydrogenase from a non-methanogenic hyperthermophilic archaeon

  • Jeong Ho Jeon
  • Jae Kyu Lim
  • Min-Sik Kim
  • Tae-Jun Yang
  • Seong-Hyuk Lee
  • Seung Seob Bae
  • Yun Jae Kim
  • Sang Hee Lee
  • Jung-Hyun Lee
  • Sung Gyun KangEmail author
  • Hyun Sook LeeEmail author
Original Paper

Abstract

The F420-reducing hydrogenase has been known as a key enzyme in methanogenesis. Its homologs have been identified in non-methanogenic hyperthermophilic archaea, including Thermococcus onnurineus NA1, but neither physiological function nor biochemical properties have been reported to date. The enzyme of T. onnurineus NA1 was distinguished from those of other methanogens and the members of the family Desulfurobacteriaceae with respect to the phylogenetic distribution of the α and β subunits, organization of frhAGB genes and conservation of F420-coordinating residues. RT-qPCR and Western blot analyses revealed frhA gene is not silent but is expressed in T. onnurineus NA1 grown in the presence of sulfur, carbon monoxide, or formate. The trimeric enzyme complex was purified to homogeneity via affinity chromatography from T. onnurineus NA1 and exhibited catalytic activity toward the electron acceptors such as viologens and flavins but not the deazaflavin coenzyme F420. This is the first biochemical study on the function of the frhAGB-encoding enzyme from a non-methanogenic archaea.

Keywords

F420-reducing hydrogenase Thermococcus onnurineus NA1 FrhAGB 

Notes

Acknowledgments

This work was supported by the KIOST in-house programs (PE99212 and PE99263) and the Development of Biohydrogen Production Technology Using the Hyperthermophilic Archaea program of the Ministry of Land, Transport, and Maritime Affairs of the Republic of South Korea. The research was also supported by a grant from the National Research Lab Program (2011-0027928) through the National Research Foundation of Korea (NRF), with funds provided by the Ministry of Science, ICT & Future Planning. We would like to thank Dr. William Whitman (University of Georgia) for kindly providing the F420 coenzyme.

Supplementary material

792_2014_689_MOESM1_ESM.doc (1.5 mb)
Supplementary material 1 (DOC 1548 kb)

References

  1. Alex LA, Reeve JN, Orme-Johnson WH, Walsh CT (1990) Cloning, sequence determination, and expression of the genes encoding the subunits of the nickel-containing 8-hydroxy-5-deazaflavin reducing hydrogenase from Methanobacterium thermoautotrophicum delta H. Biochemistry 29:7237–7244PubMedCrossRefGoogle Scholar
  2. Aufhammer SW, Warkentin E, Berk H, Shima S, Thauer RK, Ermler U (2004) Coenzyme binding in F420-dependent secondary alcohol dehydrogenase, a member of the bacterial luciferase family. Structure 12:361–370PubMedCrossRefGoogle Scholar
  3. Aufhammer SW, Warkentin E, Ermler U, Hagemeier CH, Thauer RK, Shima S (2005) Crystal structure of methylenetetrahydromethanopterin reductase (Mer) in complex with coenzyme F420: architecture of the F420/FMN binding site of enzymes within the nonprolyl cis-peptide containing bacterial luciferase family. Protein Sci 14:1840–1849PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bae SS, Kim YJ, Yang SH, Lim JK, Jeon JH, Lee HS, Kang SG, Kim SJ, Lee JH (2006) Thermococcus onnurineus sp nov., a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent area at the PACMANUS field. J Microbiol Biotechnol 16:1826–1831Google Scholar
  5. Balch WE, Wolfe RS (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl Environ Microbiol 32:781–791PubMedCentralPubMedGoogle Scholar
  6. Baron SF, Ferry JG (1989) Purification and properties of the membrane-associated coenzyme F420-reducing hydrogenase from Methanobacterium formicicum. J Bacteriol 171:3846–3853PubMedCentralPubMedGoogle Scholar
  7. Bashiri G, Squire CJ, Moreland NJ, Baker EN (2008) Crystal structures of F420-dependent glucose-6-phosphate dehydrogenase FGD1 involved in the activation of the anti-tuberculosis drug candidate PA-824 reveal the basis of coenzyme and substrate binding. J Biol Chem 283:17531–17541PubMedCrossRefGoogle Scholar
  8. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190PubMedCentralPubMedCrossRefGoogle Scholar
  9. Eirich LD, Vogels GD, Wolfe RS (1978) Proposed structure for coenzyme F420 from Methanobacterium. Biochemistry 17:4583–4593PubMedCrossRefGoogle Scholar
  10. Erkel C, Kube M, Reinhardt R, Liesack W (2006) Genome of rice cluster I archaea–the key methane producers in the rice rhizosphere. Science 313:370–372PubMedCrossRefGoogle Scholar
  11. Fiebig K, Friedrich B (1989) Purification of the F420-reducing hydrogenase from Methanosarcina barkeri (strain Fusaro). Eur J Biochem 184:79–88PubMedCrossRefGoogle Scholar
  12. Fox JA, Livingston DJ, Orme-Johnson WH, Walsh CT (1987) 8-Hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum: 1. Purification and characterization. Biochemistry 26:4219–4227PubMedCrossRefGoogle Scholar
  13. Giovannelli D, Ricci J, Pérez-Rodríguez I, Hugler M, O’Brien C, Keddis R, Grosche A, Goodwin L, Bruce D, Davenport KW, Detter C, Han J, Han S, Ivanova N, Land ML, Mikhailova N, Nolan M, Pitluck S, Tapia R, Woyke T, Vetriani C (2012) Complete genome sequence of Thermovibrio ammonificans HB-1(T), a thermophilic, chemolithoautotrophic bacterium isolated from a deep-sea hydrothermal vent. Stand Genomic Sci 7:82–90PubMedCentralPubMedCrossRefGoogle Scholar
  14. Göker M, Daligault H, Mwirichia R, Lapidus A, Lucas S, Deshpande S, Pagani I, Tapia R, Cheng JF, Goodwin L, Pitluck S, Liolios K, Ivanova N, Mavromatis K, Mikhailova N, Pati A, Chen A, Palaniappan K, Han C, Land M, Hauser L, Pan C, Brambilla EM, Rohde M, Spring S, Sikorski J, Wirth R, Detter JC, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP (2011) Complete genome sequence of the thermophilic sulfur-reducer Desulfurobacterium thermolithotrophum type strain (BSA(T)) from a deep-sea hydrothermal vent. Stand Genomic Sci 5:407–415PubMedCentralPubMedCrossRefGoogle Scholar
  15. Graham DE, White RH (2002) Elucidation of methanogenic coenzyme biosyntheses: from spectroscopy to genomics. Nat Prod Rep 19:133–147PubMedCrossRefGoogle Scholar
  16. Halboth S, Klein A (1992) Methanococcus voltae harbors four gene clusters potentially encoding two [NiFe] and two [NiFeSe] hydrogenases, each of the cofactor F420-reducing or F420-non-reducing types. Mol Gen Genet 233:217–224PubMedCrossRefGoogle Scholar
  17. Holden JF, Takai K, Summit M, Bolton S, Zyskowski J, Baross JA (2001) Diversity among three novel groups of hyperthermophilic deep-sea Thermococcus species from three sites in the northeastern Pacific Ocean. FEMS Microbiol Ecol 36:51–60PubMedCrossRefGoogle Scholar
  18. Jacobson FS, Daniels L, Fox JA, Walsh CT, Orme-Johnson WH (1982) Purification and properties of an 8-hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum. J Biol Chem 257:3385–3388PubMedGoogle Scholar
  19. Jun X, Lupeng L, Minjuan X, Oger P, Fengping W, Jebbar M, Xiang X (2011) Complete genome sequence of the obligate piezophilic hyperthermophilic archaeon Pyrococcus yayanosii CH1. J Bacteriol 193:4297–4298PubMedCentralPubMedCrossRefGoogle Scholar
  20. Jung A, Domratcheva T, Tarutina M, Wu Q, Ko WH, Shoeman RL, Gomelsky M, Gardner KH, Schlichting I (2005) Structure of a bacterial BLUF photoreceptor: insights into blue light-mediated signal transduction. Proc Natl Acad Sci USA 102:12350–12355PubMedCentralPubMedCrossRefGoogle Scholar
  21. Jung JH, Holden JF, Seo DH, Park KH, Shin H, Ryu S, Lee JH, Park CS (2012) Complete genome sequence of the hyperthermophilic archaeon Thermococcus sp. strain CL1, isolated from a Paralvinella sp. polychaete worm collected from a hydrothermal vent. J Bacteriol 194:4769–4770PubMedCentralPubMedCrossRefGoogle Scholar
  22. Kim YJ, Lee HS, Kim ES, Bae SS, Lim JK, Matsumi R, Lebedinsky AV, Sokolova TG, Kozhevnikova DA, Cha SS, Kim SJ, Kwon KK, Imanaka T, Atomi H, Bonch-Osmolovskaya EA, Lee JH, Kang SG (2010) Formate-driven growth coupled with H2 production. Nature 467:352–355PubMedCrossRefGoogle Scholar
  23. Kim MS, Bae SS, Kim YJ, Kim TW, Lim JK, Lee SH, Choi AR, Jeon JH, Lee JH, Lee HS, Kang SG (2013) CO-dependent H2 production by genetically engineered Thermococcus onnurineus NA1. Appl Environ Microbiol 79:2048–2053PubMedCentralPubMedCrossRefGoogle Scholar
  24. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  25. Lee HS, Kang SG, Bae SS, Lim JK, Cho Y, Kim YJ, Jeon JH, Cha SS, Kwon KK, Kim HT, Park CJ, Lee HW, Kim SI, Chun J, Colwell RR, Kim SJ, Lee JH (2008) The complete genome sequence of Thermococcus onnurineus NA1 reveals a mixed heterotrophic and carboxydotrophic metabolism. J Bacteriol 190:7491–7499PubMedCentralPubMedCrossRefGoogle Scholar
  26. Lü Z, Lu Y (2012) Complete genome sequence of a thermophilic methanogen, Methanocella conradii HZ254, isolated from Chinese rice field soil. J Bacteriol 194:2398–2399PubMedCentralPubMedCrossRefGoogle Scholar
  27. Lu Y, Lueders T, Friedrich MW, Conrad R (2005) Detecting active methanogenic populations on rice roots using stable isotope probing. Environ Microbiol 7:326–336PubMedCrossRefGoogle Scholar
  28. Lupa B, Hendrickson EL, Leigh JA, Witman WB (2008) Formate-dependent H2 production by the mesophilic methanogen Methanococcus maripaludis. Appl Environ Microbiol 74:6584–6590PubMedCentralPubMedCrossRefGoogle Scholar
  29. Ma K, Adams MW (2001) Hydrogenases I and II from Pyrococcus furiosus. Methods Enzymol 331:208–216PubMedCrossRefGoogle Scholar
  30. Matsumi R, Manabe K, Fukui T, Atomi H, Imanaka T (2007) Disruption of a sugar transporter gene cluster in a hyperthermophilic archaeon using a host-marker system based on antibiotic resistance. J Bacteriol 189:2683–2691PubMedCentralPubMedCrossRefGoogle Scholar
  31. Michel R, Massanz C, Kostka S, Richter M, Fiebig K (1995) Biochemical characterization of the 8-hydroxy-5-deazaflavin-reactive hydrogenase from Methanosarcina barkeri Fusaro. Eur J Biochem 233:727–735PubMedCrossRefGoogle Scholar
  32. Mills DJ, Vitt S, Strauss M, Shima S, Vonck J (2013) De novo modeling of the F420-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy. eLife 2:e00218Google Scholar
  33. Muth E, Mörschel E, Klein A (1987) Purification and characterization of an 8-hydroxy-5-deazaflavin-reducing hydrogenase from the archaebacterium Methanococcus voltae. Eur J Biochem 169:571–577PubMedCrossRefGoogle Scholar
  34. Sakai S, Imachi H, Hanada S, Ohashi A, Harada H, Kamagata Y (2008) Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage ‘Rice Cluster I’, and proposal of the new archaeal order Methanocellales ord. nov. Int J Syst Evol Microbiol 58:929–936PubMedCrossRefGoogle Scholar
  35. Sakai S, Takaki Y, Shimamura S, Sekine M, Tajima T, Kosugi H, Ichikawa N, Tasumi E, Hiraki AT, Shimizu A, Kato Y, Nishiko R, Mori K, Fujita N, Imachi H, Takai K (2011) Genome sequence of a mesophilic hydrogenotrophic methanogen Methanocella paludicola, the first cultivated representative of the order Methanocellales. PLoS One 6:e228988Google Scholar
  36. Slesarev AI, Mezhevaya KV, Makarova KS, Polushin NN, Shcherbinina OV, Shakhova VV, Belova GI, Aravind L, Natale DA, Rogozin IB, Tatusov RL, Wolf YI, Stetter KO, Malykh AG, Koonin EV, Kozyavkin SA (2002) The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc Natl Acad Sci USA 99:4644–4649PubMedCentralPubMedCrossRefGoogle Scholar
  37. Sokolova TG, Jeanthon C, Kostrikina NA, Chernyh NA, Lebedinsky AV, Stackebrandt E, Bonch-Osmolovskaya EA (2004) The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8:317–323PubMedCrossRefGoogle Scholar
  38. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  39. Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. 1998 Marjory Stephenson Prize Lecture. Microbiology 144:2377–2406PubMedCrossRefGoogle Scholar
  40. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180PubMedCentralPubMedGoogle Scholar
  41. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCentralPubMedCrossRefGoogle Scholar
  42. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501PubMedCrossRefGoogle Scholar
  43. Walsh C (1980) Flavin coenzymes: at the crossroads of biological redox chemistry. Acc Chem Res 13:148–155CrossRefGoogle Scholar
  44. Walsh C (1986) Naturally occurring 5-deazaflavin coenzymes: biological redox roles. Acc Chem Res 19:216–221CrossRefGoogle Scholar
  45. Wang X, Gao Z, Xu X, Ruan L (2011) Complete genome sequence of Thermococcus sp. strain 4557, a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent area. J Bacteriol 193:5544–5545PubMedCentralPubMedCrossRefGoogle Scholar
  46. White RH (2001) Biosynthesis of the methanogenic cofactors. Vitam Horm 61:299–337PubMedCrossRefGoogle Scholar
  47. Yuan Y, Conrad R, Lu Y (2009) Responses of methanogenic archaeal community to oxygen exposure in rice field soil. Environ Microbiol Rep 1:347–354PubMedCrossRefGoogle Scholar
  48. Zivanovic Y, Armengaud J, Lagorce A, Leplat C, Guerin P, Dutertre M, Anthouard V, Forterre P, Wincker P, Confalonieri F (2009) Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea. Genome Biol 10:R70PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2014

Authors and Affiliations

  • Jeong Ho Jeon
    • 1
    • 3
  • Jae Kyu Lim
    • 1
  • Min-Sik Kim
    • 1
  • Tae-Jun Yang
    • 1
  • Seong-Hyuk Lee
    • 1
    • 2
  • Seung Seob Bae
    • 1
    • 2
  • Yun Jae Kim
    • 1
  • Sang Hee Lee
    • 3
  • Jung-Hyun Lee
    • 1
    • 2
  • Sung Gyun Kang
    • 1
    • 2
    Email author
  • Hyun Sook Lee
    • 1
    • 2
    Email author
  1. 1.Marine Biotechnology Research DivisionKorea Institute of Ocean Science and TechnologyAnsanSouth Korea
  2. 2.Department of Marine BiotechnologyKorea University of Science and TechnologyDaejeonSouth Korea
  3. 3.Department of Biological Sciences, National Leading Research LaboratoryMyongji UniversityYonginSouth Korea

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