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PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference

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Abstract

Methanol dehydrogenase (MDH) catalyzes the first step in methanol use by methylotrophic bacteria and the second step in methane conversion by methanotrophs. Gram-negative bacteria possess an MDH with pyrroloquinoline quinone (PQQ) as its catalytic center. This MDH belongs to the broad class of eight-bladed β propeller quinoproteins, which comprise a range of other alcohol and aldehyde dehydrogenases. A well-investigated MDH is the heterotetrameric MxaFI-MDH, which is composed of two large catalytic subunits (MxaF) and two small subunits (MxaI). MxaFI-MDHs bind calcium as a cofactor that assists PQQ in catalysis. Genomic analyses indicated the existence of another MDH distantly related to the MxaFI-MDHs. Recently, several of these so-called XoxF-MDHs have been isolated. XoxF-MDHs described thus far are homodimeric proteins lacking the small subunit and possess a rare-earth element (REE) instead of calcium. The presence of such REE may confer XoxF-MDHs a superior catalytic efficiency. Moreover, XoxF-MDHs are able to oxidize methanol to formate, rather than to formaldehyde as MxaFI-MDHs do. While structures of MxaFI- and XoxF-MDH are conserved, also regarding the binding of PQQ, the accommodation of a REE requires the presence of a specific aspartate residue near the catalytic site. XoxF-MDHs containing such REE-binding motif are abundantly present in genomes of methylotrophic and methanotrophic microorganisms and also in organisms that hitherto are not known for such lifestyle. Moreover, sequence analyses suggest that XoxF-MDHs represent only a small part of putative REE-containing quinoproteins, together covering an unexploited potential of metabolic functions.

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References

  • Abanda-Nkpwatt D, Müsch M, Tschiersch J, Boettner M, Schwab W (2006) Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot 57(15):4025–4032

    CAS  PubMed  Google Scholar 

  • Adachi O, Fujii Y, Ghaly MF, Toyama H, Shinagawa E, Matsushita K (2001) Membrane-bound quinoprotein d-arabitol dehydrogenase of Gluconobacter suboxydans IFO 3257: a versatile enzyme for the oxidative fermentation of various ketoses. Biosci Biotechnol Biochem 65(12):2755–2762

    CAS  PubMed  Google Scholar 

  • Afolabi PR, Mohammed F, Amaratunga K, Majekodunmi O, Dales SL, Gill R, Thompson D, Cooper JB, Wood SP, Goodwin PM, Anthony C (2001) Site-directed mutagenesis and X-ray crystallography of the PQQ-containing quinoprotein methanol dehydrogenase and its electron acceptor, cytochrome c L. Biochemistry 40(33):9799–9809

    CAS  PubMed  Google Scholar 

  • Anderson DJ, Morris CJ, Nunn DN, Anthony C, Lidstrom ME (1990) Nucleotide sequence of the Methylobacterium extorquens AM1 moxF and moxJ genes involved in methanol oxidation. Gene 90(1):173–176

    CAS  PubMed  Google Scholar 

  • Anthony C (1982) The Biochemistry of Methylotrophs. Academic Press, London UK

    Google Scholar 

  • Anthony C (1992) The c-type cytochromes of methylotrophic bacteria. Biochim Biophys Acta 1099(1):1–15

    CAS  PubMed  Google Scholar 

  • Anthony C (1996) Quinoprotein-catalysed reactions. Biochem J 320:697–711

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anthony C (2004) The quinoprotein dehydrogenases for methanol and glucose. Arch Biochem Biophys 428(1):2–9

    CAS  PubMed  Google Scholar 

  • Anthony C, Ghosh M (1998) The structure and function of the PQQ-containing quinoprotein dehydrogenases. Prog Biophys Mol Biol 69(1):1–21

    CAS  PubMed  Google Scholar 

  • Anthony C, Ghosh M, Blake CC (1994) The structure and function of methanol dehydrogenase and related quinoproteins containing pyrrolo-quinoline quinone. Biochem J 304:665–674

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anthony C, Williams P (2003) The structure and mechanism of methanol dehydrogenase. Biochim Biophys Acta 1647(1–2):18–23

    CAS  PubMed  Google Scholar 

  • Anthony C, Zatman LJ (1964a) The microbial oxidation of methanol. 1. Isolation and properties of Pseudomonas sp. M27. Biochem J 92(3):609–614

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anthony C, Zatman LJ (1964b) The microbial oxidation of methanol. 2. The methanol-oxidizing enzyme of Pseudomonas sp. M 27. Biochem J 92(3):614–621

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anthony C, Zatman LJ (1967a) The microbial oxidation of methanol. Purification and properties of the alcohol dehydrogenase of Pseudomonas sp. M27. Biochem J 104(3):953–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anthony C, Zatman LJ (1967b) The microbial oxidation of methanol. The prosthetic group of the alcohol dehydrogenase of Pseudomonas sp. M27: a new oxidoreductase prosthetic group. Biochem J 104(3):960–969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Attwood MM (1990) Formaldehyde dehydrogenases from methylotrophs. Methods Enzymol 188:314–324

    CAS  Google Scholar 

  • Barber RD, Donohue TJ (1998) Function of a glutathione-dependent formaldehyde dehydrogenase in Rhodobacter sphaeroides formaldehyde oxidation and assimilation. Biochemistry 37(2):530–537

    CAS  PubMed  Google Scholar 

  • Blake CC, Ghosh M, Harlos K, Avezoux A, Anthony C (1994) The active site of methanol dehydrogenase contains a disulphide bridge between adjacent cysteine residues. Nat Struct Biol 1(2):102–105

    CAS  PubMed  Google Scholar 

  • Bosch G, Wang T, Latypova E, Kalyuzhnaya MG, Hackett M, Chistoserdova L (2009) Insights into the physiology of Methylotenera mobilis as revealed by metagenome-based shotgun proteomic analysis. Microbiology 155:1103–1110

    CAS  PubMed  Google Scholar 

  • Chen ZW, Matsushita K, Yamashita T, Fujii TA, Toyama H, Adachi O, Bellamy HD, Mathews FS (2002) Structure at 1.9 A resolution of a quinohemoprotein alcohol dehydrogenase from Pseudomonas putida HK5. Structure 10(6):837–849

    CAS  PubMed  Google Scholar 

  • Cherney MM, Zhang Y, Solomonson M, Weiner JH, James MN (2010) Crystal structure of sulfide:quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J Mol Biol 398(2):292–305

    CAS  PubMed  Google Scholar 

  • Chistoserdova L (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13(10):2603–2622

    CAS  PubMed  Google Scholar 

  • Chistoserdova L, Chen SW, Lapidus A, Lidstrom ME (2003) Methylotrophy in Methylobacterium extorquens AM1 from a genomic point of view. J Bacteriol 185(10):2980–2987

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chistoserdova L, Kalyuzhnaya MG, Lidstrom ME (2009) The expanding world of methylotrophic metabolism. Annu Rev Microbiol 63:477–499

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chistoserdova L, Lapidus A, Han C, Goodwin L, Saunders L, Brettin T, Tapia R, Gilna P, Lucas S, Richardson PM, Lidstrom ME (2007) Genome of Methylobacillus flagellatus, molecular basis for obligate methylotrophy, and polyphyletic origin of methylotrophy. J Bacteriol 189(11):4020–4027

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chistoserdova LV, Lidstrom ME (1994a) Genetics of the serine cycle in Methylobacterium extorquens AM1: cloning, sequence, mutation, and physiological effect of glyA, the gene for serine hydroxymethyltransferase. J Bacteriol 176(21):6759–6762

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chistoserdova LV, Lidstrom ME (1994b) Genetics of the serine cycle in Methylobacterium extorquens AM1: identification, sequence, and mutation of three new genes involved in C1 assimilation, orf4, mtkA, and mtkB. J Bacteriol 176(23):7398–7404

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chistoserdova L, Lidstrom ME (1997) Molecular and mutational analysis of a DNA region separating two methylotrophy gene clusters in Methylobacterium extorquens AM1. Microbiology 143:1729–1736

    CAS  PubMed  Google Scholar 

  • Chistoserdova L, Vorholt JA, Thauer RK, Lidstrom ME (1998) C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science 281(5373):99–102

    CAS  PubMed  Google Scholar 

  • Choi DW, Kunz RC, Boyd ES, Semrau JD, Antholine WE, Han JI, Zahn JA, Boyd JM, de la Mora AM, DiSpirito AA (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase complex from Methylococcus capsulatus Bath. J Bacteriol 185(19):5755–5764

    CAS  PubMed Central  PubMed  Google Scholar 

  • Choi JM, Kim HG, Kim JS, Youn HS, Eom SH, Yu SL, Kim SW, Lee SH (2011) Purification, crystallization and preliminary X-ray crystallographic analysis of a methanol dehydrogenase from the marine bacterium Methylophaga aminisulfidivorans MP(T). Acta Crystallogr Sect F: Struct Biol Cryst Commun 67:513–516

    CAS  Google Scholar 

  • Choi O, Kim J, Kim JG, Jeong Y, Moon JS, Park CS, Hwang I (2008) Pyrroloquinoline quinone is a plant growth promotion factor produced by Pseudomonas fluorescens B16. Plant Physiol 146(2):657–668

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cook SA, Shiemke AK (2002) Evidence that a type-2 NADH:quinone oxidoreductase mediates electron transfer to particulate methane monooxygenase in Methylococcus capsulatus. Arch Biochem Biophys 398(1):32–40

    CAS  PubMed  Google Scholar 

  • Crowther GJ, Kosály G, Lidstrom ME (2008) Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J Bacteriol 190(14):5057–5062

    CAS  PubMed Central  PubMed  Google Scholar 

  • Culpepper MA, Rosenzweig AC (2012) Architecture and active site of particulate methane monooxygenase. Crit Rev Biochem Mol Biol 47(6):483–492

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davidson VL (2004) Electron transfer in quinoproteins. Arch Biochem Biophys 428(1):32–40

    CAS  PubMed  Google Scholar 

  • DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA

    Google Scholar 

  • Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106(38):16428–16433

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dewanti AR, Duine JA (2000) Ca2+-assisted, direct hydride transfer, and rate-determining tautomerization of C5-reduced PQQ to PQQH2, in the oxidation of beta-d-glucose by soluble, quinoprotein glucose dehydrogenase. Biochemistry 39(31):9384–9392

    CAS  PubMed  Google Scholar 

  • Dijkstra M, Van den Tweel WJJ, De Bont JAM, Frank J, Jzn DJA (1985) Monomeric and dimeric alcohol dehydrogenase from alcohol-grown Pseudomonas BB1. J Gen Microbiol 131:3163–3169

    CAS  Google Scholar 

  • Dunfield PF, Yuryev A, Senin P, Smirnova AV, Stott MB, Hou S, Ly B, Saw JH, Zhou Z, Ren Y, Wang J, Mountain BW, Crowe MA, Weatherby TM, Bodelier PL, Liesack W, Feng L, Wang L, Alam M (2007) Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature 450(7171):879–882

    CAS  PubMed  Google Scholar 

  • Erb TJ, Berg IA, Brecht V, Müller M, Fuchs G, Alber BE (2007) Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: the ethylmalonyl-CoA pathway. Proc Natl Acad Sci U S A 104(25):10631–10636

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJM, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MSM, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464(7288):543–548

    CAS  PubMed  Google Scholar 

  • Fall R, Benson AA (1996) Leaf methanol—the simplest natural product from plants. Trends Plant Sci 1:296–301

    Google Scholar 

  • Fitriyanto NA, Fushimi M, Matsunaga M, Pertiwiningrum A, Iwama T, Kawai K (2011) Molecular structure and gene analysis of Ce3+-induced methanol dehydrogenase of Bradyrhizobium sp. MAFF211645. J Biosci Bioeng 111(6):613–617

    CAS  PubMed  Google Scholar 

  • Ghosh M, Anthony C, Harlos K, Goodwin MG, Blake C (1995) The refined structure of the quinoprotein methanol dehydrogenase from Methylobacterium extorquens at 1.94 A. Structure 3(2):177–187

    CAS  PubMed  Google Scholar 

  • Ghosh M, Avezoux A, Anthony C, Harlos K, Blake CC (1994) X-ray structure of PQQ-dependent methanol dehydrogenase. EXS 71:251–260

    CAS  PubMed  Google Scholar 

  • Ghosh R, Quayle JR (1981) Purification and properties of the methanol dehydrogenase from Methylophilus methylotrophus. Biochem J 199(1):245–250

    CAS  PubMed Central  PubMed  Google Scholar 

  • Giovannoni SJ, Hayakawa DH, Tripp HJ, Stingl U, Givan SA, Cho JC, Oh HM, Kitner JB, Vergin KL, Rappé MS (2008) The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10(7):1771–1782

  • Gliese N, Khodaverdi V, Görisch H (2010) The PQQ biosynthetic operons and their transcriptional regulation in Pseudomonas aeruginosa. Arch Microbiol 192(1):1–14

    CAS  PubMed  Google Scholar 

  • Gómez-Manzo S, Contreras-Zentella M, González-Valdez A, Sosa-Torres M, Arreguín-Espinoza R, Escamilla-Marván E (2008) The PQQ-alcohol dehydrogenase of Gluconacetobacter diazotrophicus. Int J Food Microbiol 125(1):71–78

    PubMed  Google Scholar 

  • Goodwin MG, Anthony C (1996) Characterization of a novel methanol dehydrogenase containing a Ba2+ ion at the active site. Biochem J 318:673–679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Goosen N, Huinen RGM, Vandeputte P (1992) A 24-amino-acid polypeptide is essential for the biosynthesis of the coenzyme pyrrolo-quinoline-quinone. J Bacteriol 174(4):1426–1427

    CAS  PubMed Central  PubMed  Google Scholar 

  • Görisch H, Rupp M (1989) Quinoprotein ethanol dehydrogenase from Pseudomonas. Antonie Van Leeuwenhoek 56(1):35–45

    PubMed  Google Scholar 

  • Groen BW, van Kleef MA, Duine JA (1986) Quinohaemoprotein alcohol dehydrogenase apoenzyme from Pseudomonas testosteroni. Biochem J 234(3):611–615

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grosse S, Voigt C, Wendlandt K-D, Kleber HP (1998) Purification and properties of methanol dehydrogenase from Methylosinus sp. WI 14. J Basic Microbiol 38(3):189–196

    CAS  PubMed  Google Scholar 

  • Grosse S, Wendlandt KD, Kleber HP (1997) Purification and properties of methanol dehydrogenase from Methylocystis sp. GB 25. J Basic Microbiol 37(4):269–279

    CAS  PubMed  Google Scholar 

  • Hagemeier CH, Chistoserdova L, Lidstrom ME, Thauer RK, Vorholt JA (2000) Characterization of a second methylene tetrahydromethanopterin dehydrogenase from Methylobacterium extorquens AM1. Eur J Biochem 267(12):3762–3769

    CAS  PubMed  Google Scholar 

  • Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241

    CAS  PubMed  Google Scholar 

  • Hektor HJ, Kloosterman H, Dijkhuizen L (2000) Nicotinoprotein methanol dehydrogenase enzymes in Gram-positive methylotrophic bacteria. J Mol Catal B 8(1):103–109

    CAS  Google Scholar 

  • Hektor HJ, Kloosterman H, Dijkhuizen L (2002) Identification of a magnesium-dependent NAD(P)(H)-binding domain in the nicotinoprotein methanol dehydrogenase from Bacillus methanolicus. J Biol Chem 277(49):46966–46973

    CAS  PubMed  Google Scholar 

  • Hibi Y, Asai K, Arafuka H, Hamajima M, Iwama T, Kawai K (2011) Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans. J Biosci Bioeng 111(5):547–549

    CAS  PubMed  Google Scholar 

  • Hou S, Makarova KS, Saw JH, Senin P, Ly BV, Zhou Z, Ren Y, Wang J, Galperin MY, Omelchenko MV, Wolf YI, Yutin N, Koonin EV, Stott MB, Mountain BW, Crowe MA, Smirnova AV, Dunfield PF, Feng L, Wang L, Alam M (2008) Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct 3:26

    PubMed Central  PubMed  Google Scholar 

  • Islam T, Jensen S, Reigstad LJ, Larsen Ø, Birkeland NK (2008) Methane oxidation at 55 degrees C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc Natl Acad Sci U S A 105(1):300–304

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kalyuzhnaya MG, Hristova KR, Lidstrom ME, Chistoserdova L (2008a) Characterization of a novel methanol dehydrogenase in representatives of Burkholderiales: implications for environmental detection of methylotrophy and evidence for convergent evolution. J Bacteriol 190(11):3817–3823

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kalyuzhnaya MG, Lapidus A, Ivanova N, Copeland AC, McHardy AC, Szeto E, Salamov A, Grigoriev IV, Suciu D, Levine SR, Markowitz VM, Rigoutsos I, Tringe SG, Bruce DC, Richardson PM, Lidstrom ME, Chistoserdova L (2008b) High-resolution metagenomics targets specific functional types in complex microbial communities. Nat Biotechnol 26(9):1029–1034

    CAS  PubMed  Google Scholar 

  • Kalyuzhnaya MG, Yang S, Rozova ON, Smalley NE, Clubb J, Lamb A, Gowda GA, Raftery D, Fu Y, Bringel F, Vuilleumier S, Beck DA, Trotsenko YA, Khmelenina VN, Lidstrom ME (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4:2785. doi:10.1038/ncomms3785

    CAS  PubMed  Google Scholar 

  • Keitel T, Diehl A, Knaute T, Stezowski JJ, Höhne W, Görisch H (2000) X-ray structure of the quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosa: basis of substrate specificity. J Mol Biol 297(4):961–974

    CAS  PubMed  Google Scholar 

  • Khadem AF, van Teeseling MC, van Niftrik L, Jetten MSM, Op den Camp HJM, Pol A (2012a) Genomic and physiological analysis of carbon storage in the verrucomicrobial methanotroph “Ca. Methylacidiphilum fumariolicum” SolV. Front Microbiol 3:345

    PubMed Central  PubMed  Google Scholar 

  • Khadem AF, Wieczorek AS, Pol A, Vuilleumier S, Harhangi HR, Dunfield PF, Kalyuzhnaya MG, Murrell JC, Francoijs KJ, Stunnenberg HG, Stein LY, DiSpirito AA, Semrau JD, Lajus A, Médigue C, Klotz MG, Jetten MSM, Op den Camp HJM (2012b) Draft genome sequence of the volcano-inhabiting thermoacidophilic methanotroph Methylacidiphilum fumariolicum strain SolV. J Bacteriol 194(14):3729–3730

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim HG, Han GH, Kim D, Choi JS, Kim SW (2012) Comparative analysis of two types of methanol dehydrogenase from Methylophaga aminisulfidivorans MPT grown on methanol. J Basic Microbiol 52(2):141–149

    CAS  PubMed  Google Scholar 

  • Klein CR, Kesseler FP, Perrei C, Frank J, Duine JA, Schwartz AC (1994) A novel dye-linked formaldehyde dehydrogenase with some properties indicating the presence of a protein-bound redox-active quinone cofactor. Biochem J 301:289–295

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kopp DA, Lippard SJ (2002) Soluble methane monooxygenase: activation of dioxygen and methane. Curr Opin Chem Biol 6(5):568–576

    CAS  PubMed  Google Scholar 

  • Lapidus A, Clum A, Labutti K, Kaluzhnaya MG, Lim S, Beck DA, Glavina Del Rio T, Nolan M, Mavromatis K, Huntemann M, Lucas S, Lidstrom ME, Ivanova N, Chistoserdova L (2011) Genomes of three methylotrophs from a single niche reveal the genetic and metabolic divergence of the methylophilaceae. J Bacteriol 193(15):3757–3764

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lidstrom ME, Anthony C, Biville F, Gasser F, Goodwin P, Hanson RS, Harms N (1994) New unified nomenclature for genes involved in the oxidation of methanol in Gram-negative bacteria. FEMS Microbiol Lett 117(1):103–106

    CAS  PubMed  Google Scholar 

  • Marcia M, Ermler U, Peng G, Michel H (2009) The structure of Aquifex aeolicus sulfide:quinone oxidoreductase, a basis to understand sulfide detoxification and respiration. Proc Natl Acad Sci U S A 106(24):9625–9630

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marcia M, Ermler U, Peng G, Michel H (2010) A new structure-based classification of sulfide:quinone oxidoreductases. Proteins 78(5):1073–1083

    CAS  PubMed  Google Scholar 

  • Mackenzie C, Choudhary M, Larimer FW, Predki PF, Stilwagen S, Armitage JP, Barber RD, Donohue TJ, Hosler JP, Newman JE, Shapleigh JP, Sockett RE, Zeilstra-Ryalls J, Kaplan S (2001) The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res 70(1):19–41

    CAS  PubMed  Google Scholar 

  • Matsushita K, Fujii Y, Ano Y, Toyama H, Shinjoh M, Tomiyama N, Miyazaki T, Sugisawa T, Hoshino T, Adachi O (2003) 5-keto-d-gluconate production is catalyzed by a quinoprotein glycerol dehydrogenase, major polyol dehydrogenase, in Gluconobacter species. Appl Environ Microbiol 69(4):1959–1966

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matsushita K, Takahashi K, Adachi O (1993) A novel quinoprotein methanol dehydrogenase containing an additional 32-kilodalton peptide purified from Acetobacter methanolicus: Identification of the peptide as a MoxJ product. Biochemistry 32(21):5576–5582

    CAS  PubMed  Google Scholar 

  • Matsushita K, Toyama H, Yamada M, Adachi O (2002) Quinoproteins: structure, function, and biotechnological applications. Appl Microbiol Biotechnol 58(1):13–22

    CAS  PubMed  Google Scholar 

  • Mennenga B, Kay CW, Görisch H (2009) Quinoprotein ethanol dehydrogenase from Pseudomonas aeruginosa: the unusual disulfide ring formed by adjacent cysteine residues is essential for efficient electron transfer to cytochrome c550. Arch Microbiol 191(4):361–367

    CAS  PubMed  Google Scholar 

  • Moermond CT, Tijink J, van Wezel AP, Koelmans AA (2001) Distribution, speciation, and bioavailability of lanthanides in the Rhine-Meuse estuary, The Netherlands. Environ Toxicol Chem 20(9):1916–1926

  • Murray LJ, Lippard SJ (2007) Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygenases. Acc Chem Res 40(7):466–474

    CAS  PubMed  Google Scholar 

  • Myronova N, Kitmitto A, Collins RF, Miyaji A, Dalton H (2006) Three-dimensional structure determination of a protein supercomplex that oxidizes methane to formaldehyde in Methylococcus capsulatus (Bath). Biochemistry 45(39):11905–11914

    CAS  PubMed  Google Scholar 

  • Nakagawa T, Mitsui R, Tani A, Sasa K, Tashiro S, Iwama T, Hayakawa T, Kawai K (2012) A catalytic role of XoxF1 as La3+-dependent methanol dehydrogenase in Methylobacterium strain AM1. PLoS One 7:e50480

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nojiri M, Hira D, Yamaguchi K, Okajima T, Tanizawa K, Suzuki S (2006) Crystal structures of cytochrome c L and methanol dehydrogenase from Hyphomicrobium denitrificans: structural and mechanistic insights into interactions between the two proteins. Biochemistry 45(11):3481–3492

    CAS  PubMed  Google Scholar 

  • Nunn DN, Lidstrom ME (1986a) Isolation and complementation analysis of 10 methanol oxidation mutant classes and identification of the methanol dehydrogenase structural gene for Methylobacterium sp strain AM1. J Bacteriol 166(2):581–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nunn DN, Lidstrom ME (1986b) Phenotypic characterization of 10 methanol oxidation mutant classes in Methylobacterium sp strain AM1. J Bacteriol 166(2):591–597

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oubrie A, Dijkstra BW (2000) Structural requirements of pyrroloquinoline quinone dependent enzymatic reactions. Protein Sci 9(7):1265–1273

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oubrie A, Rozeboom HJ, Kalk KH, Huizinga EG, Dijkstra BW (2002) Crystal structure of quinohemoprotein alcohol dehydrogenase from Comamonas testosteroni: structural basis for substrate oxidation and electron transfer. J Biol Chem 277(5):3727–3732

    CAS  PubMed  Google Scholar 

  • Patel RN, Hou CT, Derelanko P, Felix A (1980) Purification and properties of a heme-containing aldehyde dehydrogenase from Methylosinus trichosporium. Arch Biochem Biophys 203(2):654–662

    CAS  PubMed  Google Scholar 

  • Peyraud R, Kiefer P, Christen P, Massou S, Portais JC, Vorholt JA (2009) Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc Natl Acad Sci U S A 106(12):4846–4851

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pol A, Barends TRM, Dietl A, Khadem AF, Eygensteyn J, Jetten MSM, Op den Camp HJM (2014) Rare earth metals are essential for methanotrophic life in volcanic mudpots. Environ Microbiol 16:255–264

    CAS  PubMed  Google Scholar 

  • Pol A, Heijmans K, Harhangi HR, Tedesco D, Jetten MSM, Op den Camp HJM (2007) Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature 450(7171):874–878

    CAS  PubMed  Google Scholar 

  • Pomper BK, Saurel O, Milon A, Vorholt JA (2002) Generation of formate by the formyltransferase/hydrolase complex (Fhc) from Methylobacterium extorquens AM1. FEBS Lett 523(1–3):133–137

    CAS  PubMed  Google Scholar 

  • Pomper BK, Vorholt JA, Chistoserdova L, Lidstrom ME, Thauer RK (1999) A methenyl tetrahydromethanopterin cyclohydrolase and a methenyl tetrahydrofolate cyclohydrolase in Methylobacterium extorquens AM1. Eur J Biochem 261(2):475–480

    CAS  PubMed  Google Scholar 

  • Popkin G (2013) Surprising metals found in microbes. ScienceNews. https://www.sciencenews.org/article/surprising-metals-found-microbes. Accessed 3 Januari 2014

  • Puehringer S, Metlitzky M, Schwarzenbacher R (2008) The pyrroloquinoline quinone biosynthesis pathway revisited, a structural approach. BMC Biochem 9:8

    PubMed Central  PubMed  Google Scholar 

  • Quayle JR, Pfennig N (1975) Utilization of methanol by Rhodospirillaceae. Arch Microbiol 102(3):193–198

    CAS  PubMed  Google Scholar 

  • Ras J, Van Ophem PW, Reijnders WN, Van Spanning RJ, Duine JA, Stouthamer AH, Harms N (1995) Isolation, sequencing, and mutagenesis of the gene encoding NAD- and glutathione-dependent formaldehyde dehydrogenase (GD-FALDH) from Paracoccus denitrificans, in which GD-FALDH is essential for methylotrophic growth. J Bacteriol 177(1):247–251

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rasigraf O, Kool DM, Jetten MS, Sinninghe Damsté JS, Ettwig KF (2014) Autotrophic carbon dioxide fixation via the Calvin–Benson–Bassham Cycle by the denitrifying methanotroph “Candidatus Methylomirabilis oxyfera”. Appl Environ Microbiol 80(8):2451–2460

    CAS  PubMed  Google Scholar 

  • Reddy SY, Bruice TC (2003) In silico studies of the mechanism of methanol oxidation by quinoprotein methanol dehydrogenase. J Am Chem Soc 125(27):8141–8150

    CAS  PubMed  Google Scholar 

  • Reddy SY, Bruice TC (2004) Determination of enzyme mechanisms by molecular dynamics: studies on quinoproteins, methanol dehydrogenase, and soluble glucose dehydrogenase. Protein Sci 13(8):1965–1978

    CAS  PubMed Central  PubMed  Google Scholar 

  • Richardson IW, Anthony C (1992) Characterization of mutant forms of the quinoprotein methanol dehydrogenase lacking an essential calcium ion. Biochem J 287:709–715

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sahm H, Cox RB, Quayle JR (1976) Metabolism of methanol by Rhodopseudomonas acidophila. J Gen Microbiol 94(2):313–322

    CAS  PubMed  Google Scholar 

  • Sato A, Takagi K, Kano K, Kato N, Duine JA, Ikeda T (2001) Ca2+ stabilizes the semiquinone radical of pyrroloquinoline quinone. Biochem J 357:893–898

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schmidt S, Christen P, Kiefer P, Vorholt JA (2010) Functional investigation of methanol dehydrogenase-like protein XoxF in Methylobacterium extorquens AM1. Microbiology 156:2575–2586

    CAS  PubMed  Google Scholar 

  • Shibata T, Ishii Y, Noguchi Y, Yamada H, Saito Y, Yamashita M (2001) Purification and molecular characterization of a quinoprotein alcohol dehydrogenase from Pseudogluconobacter saccharoketogenes IFO 14464. J Biosci Bioeng 92(6):524–531

    CAS  PubMed  Google Scholar 

  • Shiemke AK, Arp DJ, Sayavedra-Soto LA (2004) Inhibition of membrane-bound methane monooxygenase and ammonia monooxygenase by diphenyliodonium: implications for electron transfer. J Bacteriol 186(4):928–937

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sowell SM, Abraham PE, Shah M, Verberkmoes NC, Smith DP, Barofsky DF, Giovannoni SJ (2011) Environmental proteomics of microbial plankton in a highly productive coastal upwelling system. ISME J 5(5):856–865

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sperl GT, Forrest HS, Gibson DT (1974) Substrate specificity of the purified primary alcohol dehydrogenases from methanol-oxidizing bacteria. J Bacteriol 118(2):541–550

    CAS  PubMed Central  PubMed  Google Scholar 

  • Springer AL, Auman AJ, Lidstrom ME (1998) Sequence and characterization of mxaB, a response regulator involved in regulation of methanol oxidation, and of mxaW, a methanol-regulated gene in Methylobacterium extorquens AM1. FEMS Microbiol Lett 160(1):119–124

    CAS  PubMed  Google Scholar 

  • Springer AL, Morris CJ, Lidstrom ME (1997) Molecular analysis of mxbD and mxbM, a putative sensor-regulator pair required for oxidation of methanol in Methylobacterium extorquens AM1. Microbiology 143:1737–1744

    CAS  PubMed  Google Scholar 

  • Sugisawa T, Hoshino T (2002) Purification and properties of membrane-bound d-sorbitol dehydrogenase from Gluconobacter suboxydans IFO 3255. Biosci Biotechnol Biochem 66(1):57–64

    CAS  PubMed  Google Scholar 

  • Sy A, Timmers AC, Knief C, Vorholt JA (2005) Methylotrophic metabolism is advantageous for Methylobacterium extorquens during colonization of Medicago truncatula under competitive conditions. Appl Environ Microbiol 71(11):7245–7252

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28(10):2731–2739

    CAS  PubMed Central  PubMed  Google Scholar 

  • Toyama H, Chen ZW, Fukumoto M, Adachi O, Matsushita K, Mathews FS (2005) Molecular cloning and structural analysis of quinohemoprotein alcohol dehydrogenase ADH-IIG from Pseudomonas putida HK5. J Mol Biol 352(1):91–104

    CAS  PubMed  Google Scholar 

  • Toyama H, Fujii A, Matsushita K, Shinagawa E, Ameyama M, Adachi O (1995) Three distinct quinoprotein alcohol dehydrogenases are expressed when Pseudomonas putida is grown on different alcohols. J Bacteriol 177(9):2442–2450

    CAS  PubMed Central  PubMed  Google Scholar 

  • Toyama H, Mathews FS, Adachi O, Matsushita K (2004) Quinohemoprotein alcohol dehydrogenases: structure, function, and physiology. Arch Biochem Biophys 428(1):10–21

    CAS  PubMed  Google Scholar 

  • Van Spanning RJ, Wansell CW, De Boer T, Hazelaar MJ, Anazawa H, Harms N, Oltmann LF, Stouthamer AH (1991) Isolation and characterization of the moxJ, moxG, moxI, and moxR genes of Paracoccus denitrificans: inactivation of moxJ, moxG, and moxR and the resultant effect on methylotrophic growth. J Bacteriol 173(21):6948–6961

    PubMed Central  PubMed  Google Scholar 

  • Vangnai AS, Arp DJ, Sayavedra-Soto LA (2002) Two distinct alcohol dehydrogenases participate in butane metabolism by Pseudomonas butanovora (2002). J Bacteriol 184(7):1916–1924

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10(12):828–840

    CAS  PubMed  Google Scholar 

  • Vorholt JA, Chistoserdova L, Lidstrom ME, Thauer RK (1998) The NADP-dependent methylene tetrahydromethanopterin dehydrogenase in Methylobacterium extorquens AM1. J Bacteriol 180(20):5351–5356

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vorholt JA, Chistoserdova L, Stolyar SM, Thauer RK, Lidstrom ME (1999) Distribution of tetrahydromethanopterin-dependent enzymes in methylotrophic bacteria and phylogeny of methenyl tetrahydromethanopterin cyclohydrolases. J Bacteriol 181(18):5750–5757

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang L, Scanlan D, Kang KH, Lewis M, Nelson KE, Methé B, Wu M, Heidelberg JF, Paulsen IT, Fouts D, Ravel J, Tettelin H, Ren Q, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2:e303

    PubMed Central  PubMed  Google Scholar 

  • Weltje L, Heidenreich H, Zhu W, Wolterbeek HT, Korhammer S, de Goeij JJ, Markert B (2002) Lanthanide concentrations in freshwater plants and molluscs, related to those in surface water, pore water and sediment. A case study in The Netherlands. Sci Total Environ 286(1-3):191–214

  • White S, Boyd G, Mathews FS, Xia ZX, Dai WW, Zhang YF, Davidson VL (1993) The active site structure of the calcium-containing quinoprotein methanol dehydrogenase. Biochemistry 32(48):12955–12958

    CAS  PubMed  Google Scholar 

  • Williams PA, Coates L, Mohammed F, Gill R, Erskine PT, Coker A, Wood SP, Anthony C, Cooper JB (2005) The atomic resolution structure of methanol dehydrogenase from Methylobacterium extorquens. Acta Crystallogr D Biol Crystallogr 61:75–79

    CAS  PubMed  Google Scholar 

  • Wilson SM, Gleisten MP, Donohue TJ (2008) Identification of proteins involved in formaldehyde metabolism by Rhodobacter sphaeroides. Microbiology 154:296–305

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xia ZX, Dai WW, Xiong JP, Hao ZP, Davidson VL, White S, Mathews FS (1992) The three-dimensional structures of methanol dehydrogenase from two methylotrophic bacteria at 2.6-Å resolution. J Biol Chem 267(31):22289–22297

    CAS  PubMed  Google Scholar 

  • Xia Z, Dai W, Zhang Y, White SA, Boyd GD, Mathews FS (1996) Determination of the gene sequence and the three-dimensional structure at 2.4 angstroms resolution of methanol dehydrogenase from Methylophilus W3A1. J Mol Biol 259(3):480–501

    CAS  PubMed  Google Scholar 

  • Xia ZX, He YN, Dai WW, White SA, BoydGD MFS (1999) Detailed active site configuration of a new crystal form of methanol dehydrogenase from Methylophilus W3A1 at 1.9 Å resolution. Biochemistry 38(4):1214–1220

    CAS  PubMed  Google Scholar 

  • Xia ZX, Dai WW, He YN, White SA, Mathews FS, Davidson VL (2003) X-ray structure of methanol dehydrogenase from Paracoccus denitrificans and molecular modeling of its interactions with cytochrome c-551i. J Biol Inorg Chem 8(8):843–854

    CAS  PubMed  Google Scholar 

  • Yakushi T, Matsushita K (2010) Alcohol dehydrogenase of acetic acid bacteria: structure, mode of action, and applications in biotechnology. Appl Microbiol Biotechnol 86(5):1257–1265

    CAS  PubMed  Google Scholar 

  • Yamada M, Elias MD, Matsushita K, Migita CT, Adachi O (2003) Escherichia coli PQQ-containing quinoprotein glucose dehydrogenase: its structure comparison with other quinoproteins. Biochim Biophys Acta 1647(1–2):185–192

    CAS  PubMed  Google Scholar 

  • Yang M, Nightingale PD, Beale R, Liss PS, Blomquist B, Fairall C (2013) Atmospheric deposition of methanol over the Atlantic Ocean. Proc Natl Acad Sci U S A 110(50):20034–20039

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zahn JA, Bergmann DJ, Boyd JM, Kunz RC, DiSpirito AA (2001) Membrane-associated quinoprotein formaldehyde dehydrogenase from Methylococcus capsulatus Bath. J Bacteriol 183(23):6832–6840

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang X, Reddy SY, Bruice TC (2007) Mechanism of methanol oxidation by quinoprotein methanol dehydrogenase. Proc Natl Acad Sci U S A 104(3):745–749

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zheng YJ, Zx X, Zw C, Mathews FS, Bruice TC (2001) Catalytic mechanism of quinoprotein methanol dehydrogenase: A theoretical and X-ray crystallographic investigation. Proc Natl Acad Sci U S A 98(2):432–434

    CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge their colleagues Prof. Mike Jetten and Dr. Boran Kartal for critically reading the manuscript. The contribution by Joachim Reimann was supported by the Netherlands Organization for Scientific Research (ALW grant number 822.02.005).

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  1. Department of Microbiology, Institute of Wetland and Water Research, Radboud University Nijmegen, Heyendaalseweg 135, 6525AJ, Nijmegen, The Netherlands

    Jan T. Keltjens, Arjan Pol, Joachim Reimann & Huub J. M. Op den Camp

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  1. Jan T. Keltjens
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Keltjens, J.T., Pol, A., Reimann, J. et al. PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference. Appl Microbiol Biotechnol 98, 6163–6183 (2014). https://doi.org/10.1007/s00253-014-5766-8

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