Role of the malic enzyme in metabolism of the halotolerant methanotroph Methylotuvimicrobium alcaliphilum 20Z

Rozova, Olga N.; Mustakhimov, Ildar I.; But, Sergei Y.; Reshetnikov, Aleksandr S.; Khmelenina, Valentina N.

doi:10.1371/journal.pone.0225054

Title: Role of the malic enzyme in metabolism of the halotolerant methanotroph Methylotuvimicrobium alcaliphilum 20Z

Journal Article · 18 November 2019 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0225054 · OSTI ID:1629994

Rozova, Olga N. ^[1]; Mustakhimov, Ildar I. ^[2]; But, Sergei Y. ^[2]; Reshetnikov, Aleksandr S. ^[2];

^[2]

Russian Academy of Sciences (RAS), Moscow (Russian Federation); DOE/OSTI
Russian Academy of Sciences (RAS), Moscow (Russian Federation)

The bacteria utilizing methane as a growth substrate (methanotrophs) are important constituents of the biosphere. Methanotrophs mitigate the emission of anthropogenic and natural greenhouse gas methane to the environment and are the promising agents for future biotechnologies. Many aspects of CH₄ bioconversion by methanotrophs require further clarification. This study was aimed at characterizing the biochemical properties of the malic enzyme (Mae) from the halotolerant obligate methanotroph Methylotuvimicrobium alcaliphilum 20Z. The His₆-tagged Mae was obtained by heterologous expression in Escherichia coli BL21 (DE3) and purified by affinity metal chelating chromatography. As determined by gel filtration and non-denaturating gradient gel electrophoresis, the molecular mass of the native enzyme is 260 kDa. The homotetrameric Mae (65x4 kDa) catalyzed an irreversible NAD⁺-dependent reaction of L-malate decarboxylation into pyruvate with a specific activity of 32 ± 2 units mg^-1 and K_m value of 5.5 ± 0.8 mM for malate and 57 ± 5 μM for NAD⁺. The disruption of the mae gene by insertion mutagenesis resulted in a 20-fold increase in intracellular malate level in the mutant compared to the wild type strain. Based on both enzyme and mutant properties, we conclude that the malic enzyme is involved in the control of intracellular L-malate level in Mtm. alcaliphilum 20Z. Genomic analysis has revealed that Maes present in methanotrophs fall into two different clades in the amino acid-based phylogenetic tree, but no correlation of the division with taxonomic affiliations of the host bacteria was observed.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Sponsoring Organization:: Russian Foundation of Basic Research (RFBR); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1629994

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 11 Vol. 14; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (94)

Osmoadaptation in halophilic and alkaliphilic methanotrophs Khmelenina, Valentina N.; Kalyuzhnaya, Marina G.; Sakharovsky, Valentin G. Archives of Microbiology, Vol. 172, Issue 5 https://doi.org/10.1007/s002030050786	journal	October 1999
Does phosphoenolpyruvate carboxykinase have a role in both amino acid and carbohydrate metabolism? Lea, P. J.; Chen, Z. -H.; Leegood, R. C. Amino Acids, Vol. 20, Issue 3 https://doi.org/10.1007/s007260170041	journal	April 2001
Acetate kinase-an enzyme of the postulated phosphoketolase pathway in Methylomicrobium alcaliphilum 20Z Rozova, Olga N.; Khmelenina, Valentina N.; Gavletdinova, Juliya Z. Antonie van Leeuwenhoek, Vol. 108, Issue 4 https://doi.org/10.1007/s10482-015-0549-5	journal	August 2015
Serine-glyoxylate aminotranferases from methanotrophs using different C1-assimilation pathways But, S. Y.; Egorova, S. V.; Khmelenina, V. N. Antonie van Leeuwenhoek, Vol. 112, Issue 5 https://doi.org/10.1007/s10482-018-1208-4	journal	December 2018
The role of malic enzyme as the provider of NADPH in oleaginous microorganisms: a reappraisal and unsolved problems Ratledge, Colin Biotechnology Letters, Vol. 36, Issue 8 https://doi.org/10.1007/s10529-014-1532-3	journal	April 2014
Physiological functions of NAD- and NADP-linked malic enzymes in Escherichia coli Murai, Tadashi; Tokushige, Masanobu; Nagai, Jun Biochemical and Biophysical Research Communications, Vol. 43, Issue 4 https://doi.org/10.1016/0006-291x(71)90698-x	journal	May 1971
Functionally diverse biotin-dependent enzymes with oxaloacetate decarboxylase activity Lietzan, Adam D.; St. Maurice, Martin Archives of Biochemistry and Biophysics, Vol. 544 https://doi.org/10.1016/j.abb.2013.10.014	journal	February 2014
A methanotroph-based biorefinery: Potential scenarios for generating multiple products from a single fermentation Strong, P. J.; Kalyuzhnaya, M.; Silverman, J. Bioresource Technology, Vol. 215 https://doi.org/10.1016/j.biortech.2016.04.099	journal	September 2016
The PEP—pyruvate—oxaloacetate node as the switch point for carbon flux distribution in bacteria: We dedicate this paper to Rudolf K. Thauer, Director of the Max-Planck-Institute for Terrestrial Microbiology in Marburg, Germany, on the occasion of his 65th birthday Sauer, Uwe; Eikmanns, Bernhard J. FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.11.002	journal	September 2005
Heterologous expression of the Bacillus subtilis (natto) alanine dehydrogenase in Escherichia coli and Lactococcus lactis Ye, Wei; Huo, Guicheng; Chen, Junliang Microbiological Research, Vol. 165, Issue 4 https://doi.org/10.1016/j.micres.2009.05.008	journal	May 2010
Metabolic engineering in methanotrophic bacteria Kalyuzhnaya, Marina G.; Puri, Aaron W.; Lidstrom, Mary E. Metabolic Engineering, Vol. 29 https://doi.org/10.1016/j.ymben.2015.03.010	journal	May 2015
Phosphoketolase overexpression increases biomass and lipid yield from methane in an obligate methanotrophic biocatalyst Henard, Calvin A.; Smith, Holly K.; Guarnieri, Michael T. Metabolic Engineering, Vol. 41 https://doi.org/10.1016/j.ymben.2017.03.007	journal	May 2017
Bioconversion of methane to C-4 carboxylic acids using carbon flux through acetyl-CoA in engineered Methylomicrobium buryatense 5GB1C Garg, Shivani; Wu, Hao; Clomburg, James M. Metabolic Engineering, Vol. 48 https://doi.org/10.1016/j.ymben.2018.06.001	journal	July 2018
Genome-scale evaluation of core one-carbon metabolism in gammaproteobacterial methanotrophs grown on methane and methanol Nguyen, Anh Duc; Park, Joon Young; Hwang, In Yeub Metabolic Engineering, Vol. 57 https://doi.org/10.1016/j.ymben.2019.10.004	journal	January 2020
Coupling mechanism of the oxaloacetate decarboxylase Na+ pump Dimroth, Peter; Jockel, Petra; Schmid, Markus Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1505, Issue 1 https://doi.org/10.1016/s0005-2728(00)00272-3	journal	May 2001
Structure and Properties of Malic Enzyme from Bacillus stearothermophilus Kobayashi, K.; Doi, S.; Negoro, S. Journal of Biological Chemistry, Vol. 264, Issue 6 https://doi.org/10.1016/s0021-9258(18)94051-2	journal	February 1989
Characterization of two members of a novel malic enzyme class Voegele, Ralf T.; Mitsch, Michael J.; Finan, Turlough M. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1432, Issue 2 https://doi.org/10.1016/s0167-4838(99)00112-0	journal	July 1999
Structure and Function of Malic Enzymes, A New Class of Oxidative Decarboxylases Chang, Gu-Gang; Tong, Liang Biochemistry, Vol. 42, Issue 44 https://doi.org/10.1021/bi035251+	journal	October 2003
A distinct holoenzyme organization for two-subunit pyruvate carboxylase Choi, Philip H.; Jo, Jeanyoung; Lin, Yu-Cheng Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12713	journal	October 2016
Highly efficient methane biocatalysis revealed in a methanotrophic bacterium Kalyuzhnaya, M. G.; Yang, S.; Rozova, O. N. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3785	journal	December 2013
Chimeric Structure of the NAD(P)+- and NADP+-dependent Malic Enzymes ofRhizobium (Sinorhizobium) meliloti Mitsch, Michael J.; Voegele, Ralf T.; Cowie, Alison Journal of Biological Chemistry, Vol. 273, Issue 15 https://doi.org/10.1074/jbc.273.15.9330	journal	April 1998
Discovery of PPi-type Phosphoenolpyruvate Carboxykinase Genes in Eukaryotes and Bacteria Chiba, Yoko; Kamikawa, Ryoma; Nakada-Tsukui, Kumiko Journal of Biological Chemistry, Vol. 290, Issue 39 https://doi.org/10.1074/jbc.m115.672907	journal	September 2015
Comparison of partial malolactic enzyme gene sequences for phylogenetic analysis of some lactic acid bacteria species and relationships with the malic enzyme Groisillier, Agnès; Lonvaud-Funel, Aline International Journal of Systematic and Evolutionary Microbiology, Vol. 49, Issue 4 https://doi.org/10.1099/00207713-49-4-1417	journal	October 1999
Characterization of the pyrophosphate-dependent 6-phosphofructokinase from Methylococcus capsulatus Bath Reshetnikov, Alexander S.; Rozova, Olga N.; Khmelenina, Valentina N. FEMS Microbiology Letters, Vol. 288, Issue 2 https://doi.org/10.1111/j.1574-6968.2008.01366.x	journal	November 2008
Reassessment of the Transhydrogenase/Malate Shunt Pathway in Clostridium thermocellum ATCC 27405 through Kinetic Characterization of Malic Enzyme and Malate Dehydrogenase Taillefer, M.; Rydzak, T.; Levin, D. B. Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/aem.03360-14	journal	January 2015
Cloning of the Malic Enzyme Gene from Corynebacterium glutamicum and Role of the Enzyme in Lactate Metabolism Gourdon, Pierre; Baucher, Marie-France; Lindley, Nic D. Applied and Environmental Microbiology, Vol. 66, Issue 7 https://doi.org/10.1128/aem.66.7.2981-2987.2000	journal	July 2000
Draft Genome Sequence of “Candidatus Methylacidiphilum kamchatkense” Strain Kam1, a Thermoacidophilic Methanotrophic Verrucomicrobium Erikstad, Helge-André; Birkeland, Nils-Kåre Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomea.00065-15	journal	March 2015
Draft Genome Sequence of Methyloferula stellata AR4, an Obligate Methanotroph Possessing Only a Soluble Methane Monooxygenase Dedysh, Svetlana N.; Naumoff, Daniil G.; Vorobev, Alexey V. Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomea.01555-14	journal	March 2015
YtsJ Has the Major Physiological Role of the Four Paralogous Malic Enzyme Isoforms in Bacillus subtilis Lerondel, G.; Doan, T.; Zamboni, N. Journal of Bacteriology, Vol. 188, Issue 13 https://doi.org/10.1128/jb.00167-06	journal	June 2006
Escherichia coli Malic Enzymes: Two Isoforms with Substantial Differences in Kinetic Properties, Metabolic Regulation, and Structure Bologna, F. P.; Andreo, C. S.; Drincovich, M. F. Journal of Bacteriology, Vol. 189, Issue 16 https://doi.org/10.1128/jb.00428-07	journal	June 2007
Genome Sequence of the Haloalkaliphilic Methanotrophic Bacterium Methylomicrobium alcaliphilum 20Z Vuilleumier, S.; Khmelenina, V. N.; Bringel, F. Journal of Bacteriology, Vol. 194, Issue 2 https://doi.org/10.1128/jb.06392-11	journal	December 2011
Core Metabolism Shifts during Growth on Methanol versus Methane in the Methanotroph Methylomicrobium buryatense 5GB1 Fu, Yanfen; He, Lian; Reeve, Jennifer mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.00406-19	journal	April 2019
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/mr.60.2.439-471.1996	journal	January 1996
Properties of Malic Enzyme from the Aerobic Methanotroph Methylosinus trichosporium Rozova, O. N.; Khmelenina, V. N.; Mustakhimov, I. I. Biochemistry (Moscow), Vol. 84, Issue 4 https://doi.org/10.1134/s0006297919040060	journal	April 2019
The genomic landscape of the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV Anvar, Seyed; Frank, Jeroen; Pol, Arjan BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-914	journal	January 2014
Loss of malic enzymes leads to metabolic imbalance and altered levels of trehalose and putrescine in the bacterium Sinorhizobium meliloti Zhang, Ye; Smallbone, Laura Anne; diCenzo, George C. BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0780-x	journal	July 2016
Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1) de la Torre, Andrea; Metivier, Aisha; Chu, Frances Microbial Cell Factories, Vol. 14, Issue 1 https://doi.org/10.1186/s12934-015-0377-3	journal	November 2015
Purification and Characterization of the NADP-Malic Enzyme fromBradyrhizobium japonicumA1017 Chen, Fan; Okabe, Youichi; Osano, Kaoru Bioscience, Biotechnology, and Biochemistry, Vol. 61, Issue 2 https://doi.org/10.1271/bbb.61.384	journal	January 1997
Role of NAD+-Dependent Malate Dehydrogenase in the Metabolism of Methylomicrobium alcaliphilum 20Z and Methylosinus trichosporium OB3b Rozova, Olga; Khmelenina, Valentina; Bocharova, Ksenia Microorganisms, Vol. 3, Issue 1 https://doi.org/10.3390/microorganisms3010047	journal	February 2015
Oxaloacetate decarboxylase of Vibrio cholerae: Purification, characterization, and expression of the genes in Escherichia coli Pius, Dahinden,; Yolanda, Auchli,; Thierry, Granjon, ETH Zurich https://doi.org/10.3929/ethz-b-000033874	text	January 2005
Oxaloacetate decarboxylase of Vibrio cholerae: purification, characterization, and expression of the genes in Escherichia coli Dahinden, Pius; Auchli, Yolanda; Granjon, Thierry Archives of Microbiology, Vol. 183, Issue 2 https://doi.org/10.1007/s00203-004-0754-5	journal	January 2005
Osmoadaptation in halophilic and alkaliphilic methanotrophs Khmelenina, Valentina N.; Kalyuzhnaya, Marina G.; Sakharovsky, Valentin G. Archives of Microbiology, Vol. 172, Issue 5 https://doi.org/10.1007/s002030050786	journal	October 1999
Does phosphoenolpyruvate carboxykinase have a role in both amino acid and carbohydrate metabolism? Lea, P. J.; Chen, Z. -H.; Leegood, R. C. Amino Acids, Vol. 20, Issue 3 https://doi.org/10.1007/s007260170041	journal	April 2001
Acetate kinase-an enzyme of the postulated phosphoketolase pathway in Methylomicrobium alcaliphilum 20Z Rozova, Olga N.; Khmelenina, Valentina N.; Gavletdinova, Juliya Z. Antonie van Leeuwenhoek, Vol. 108, Issue 4 https://doi.org/10.1007/s10482-015-0549-5	journal	August 2015
Serine-glyoxylate aminotranferases from methanotrophs using different C1-assimilation pathways But, S. Y.; Egorova, S. V.; Khmelenina, V. N. Antonie van Leeuwenhoek, Vol. 112, Issue 5 https://doi.org/10.1007/s10482-018-1208-4	journal	December 2018
The role of malic enzyme as the provider of NADPH in oleaginous microorganisms: a reappraisal and unsolved problems Ratledge, Colin Biotechnology Letters, Vol. 36, Issue 8 https://doi.org/10.1007/s10529-014-1532-3	journal	April 2014
A simplified method for the quantitative assay of small amounts of protein in biologic material Schacterle, George R.; Pollack, Robert L. Analytical Biochemistry, Vol. 51, Issue 2 https://doi.org/10.1016/0003-2697(73)90523-X	journal	February 1973
Physiological functions of NAD- and NADP-linked malic enzymes in Escherichia coli Murai, Tadashi; Tokushige, Masanobu; Nagai, Jun Biochemical and Biophysical Research Communications, Vol. 43, Issue 4 https://doi.org/10.1016/0006-291X(71)90698-X	journal	May 1971
Prediction of the occurrence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint Wierenga, Rik K.; Terpstra, Peter; Hol, Wim G. J. Journal of Molecular Biology, Vol. 187, Issue 1, p. 101-107 https://doi.org/10.1016/0022-2836(86)90409-2	journal	January 1986
Coupling mechanism of the oxaloacetate decarboxylase Na+ pump Dimroth, Peter; Jockel, Petra; Schmid, Markus Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1505, Issue 1 https://doi.org/10.1016/S0005-2728(00)00272-3	journal	May 2001
Malic enzyme from archaebacterium Sulfolobus solfataricus. Purification, structure, and kinetic properties. Bartolucci, S.; Rella, R.; Guagliardi, A. Journal of Biological Chemistry, Vol. 262, Issue 16 https://doi.org/10.1016/S0021-9258(18)47628-4	journal	June 1987
Kinetic mechanism of NAD:malic enzyme from Ascaris suum in the direction of reductive carboxylation. Mallick, S.; Harris, B. G.; Cook, P. F. Journal of Biological Chemistry, Vol. 266, Issue 5 https://doi.org/10.1016/S0021-9258(18)49906-1	journal	February 1991
Structure and Properties of Malic Enzyme from Bacillus stearothermophilus Kobayashi, K.; Doi, S.; Negoro, S. Journal of Biological Chemistry, Vol. 264, Issue 6 https://doi.org/10.1016/S0021-9258(18)94051-2	journal	February 1989
Characterization of two members of a novel malic enzyme class Voegele, Ralf T.; Mitsch, Michael J.; Finan, Turlough M. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1432, Issue 2 https://doi.org/10.1016/S0167-4838(99)00112-0	journal	July 1999
Functionally diverse biotin-dependent enzymes with oxaloacetate decarboxylase activity Lietzan, Adam D.; St. Maurice, Martin Archives of Biochemistry and Biophysics, Vol. 544 https://doi.org/10.1016/j.abb.2013.10.014	journal	February 2014
A methanotroph-based biorefinery: Potential scenarios for generating multiple products from a single fermentation Strong, P. J.; Kalyuzhnaya, M.; Silverman, J. Bioresource Technology, Vol. 215 https://doi.org/10.1016/j.biortech.2016.04.099	journal	September 2016
Characterization of an oxaloacetate decarboxylase that belongs to the malic enzyme family Sender, Pablo D.; Martı́n, Mauricio G.; Peirú, Salvador FEBS Letters, Vol. 570, Issue 1-3 https://doi.org/10.1016/j.febslet.2004.06.038	journal	June 2004
Heterologous expression of the Bacillus subtilis (natto) alanine dehydrogenase in Escherichia coli and Lactococcus lactis Ye, Wei; Huo, Guicheng; Chen, Junliang Microbiological Research, Vol. 165, Issue 4 https://doi.org/10.1016/j.micres.2009.05.008	journal	May 2010
Metabolic engineering in methanotrophic bacteria Kalyuzhnaya, Marina G.; Puri, Aaron W.; Lidstrom, Mary E. Metabolic Engineering, Vol. 29 https://doi.org/10.1016/j.ymben.2015.03.010	journal	May 2015
Phosphoketolase overexpression increases biomass and lipid yield from methane in an obligate methanotrophic biocatalyst Henard, Calvin A.; Smith, Holly K.; Guarnieri, Michael T. Metabolic Engineering, Vol. 41 https://doi.org/10.1016/j.ymben.2017.03.007	journal	May 2017
The oxidative TCA cycle operates during methanotrophic growth of the Type I methanotroph Methylomicrobium buryatense 5GB1 Fu, Yanfen; Li, Yi; Lidstrom, Mary Metabolic Engineering, Vol. 42 https://doi.org/10.1016/j.ymben.2017.05.003	journal	July 2017
Bioconversion of methane to C-4 carboxylic acids using carbon flux through acetyl-CoA in engineered Methylomicrobium buryatense 5GB1C Garg, Shivani; Wu, Hao; Clomburg, James M. Metabolic Engineering, Vol. 48 https://doi.org/10.1016/j.ymben.2018.06.001	journal	July 2018
Structure and Function of Malic Enzymes, A New Class of Oxidative Decarboxylases Chang, Gu-Gang; Tong, Liang Biochemistry, Vol. 42, Issue 44 https://doi.org/10.1021/bi035251+	journal	October 2003
A distinct holoenzyme organization for two-subunit pyruvate carboxylase Choi, Philip H.; Jo, Jeanyoung; Lin, Yu-Cheng Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12713	journal	October 2016
Highly efficient methane biocatalysis revealed in a methanotrophic bacterium Kalyuzhnaya, M. G.; Yang, S.; Rozova, O. N. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3785	journal	December 2013
Author Correction: Methane utilization in Methylomicrobium alcaliphilum 20ZR: a systems approach Akberdin, Ilya R.; Thompson, Merlin; Hamilton, Richard Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-23088-w	journal	March 2018
Bioconversion of methane to lactate by an obligate methanotrophic bacterium Henard, Calvin A.; Smith, Holly; Dowe, Nancy Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep21585	journal	February 2016
Chimeric Structure of the NAD(P)+- and NADP+-dependent Malic Enzymes ofRhizobium (Sinorhizobium) meliloti Mitsch, Michael J.; Voegele, Ralf T.; Cowie, Alison Journal of Biological Chemistry, Vol. 273, Issue 15 https://doi.org/10.1074/jbc.273.15.9330	journal	April 1998
Discovery of PPi-type Phosphoenolpyruvate Carboxykinase Genes in Eukaryotes and Bacteria Chiba, Yoko; Kamikawa, Ryoma; Nakada-Tsukui, Kumiko Journal of Biological Chemistry, Vol. 290, Issue 39 https://doi.org/10.1074/jbc.M115.672907	journal	September 2015
MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0 Tamura, K.; Dudley, J.; Nei, M. Molecular Biology and Evolution, Vol. 24, Issue 8 https://doi.org/10.1093/molbev/msm092	journal	April 2007
Comparison of partial malolactic enzyme gene sequences for phylogenetic analysis of some lactic acid bacteria species and relationships with the malic enzyme Groisillier, Agnès; Lonvaud-Funel, Aline International Journal of Systematic and Evolutionary Microbiology, Vol. 49, Issue 4 https://doi.org/10.1099/00207713-49-4-1417	journal	October 1999
The Bacillus subtilis ywkA gene encodes a malic enzyme and its transcription is activated by the YufL/YufM two-component system in response to malate Doan, Thierry; Servant, Pascale; Tojo, Shigeo Microbiology, Vol. 149, Issue 9 https://doi.org/10.1099/mic.0.26256-0	journal	September 2003
Characterization of the pyrophosphate-dependent 6-phosphofructokinase from Methylococcus capsulatus Bath Reshetnikov, Alexander S.; Rozova, Olga N.; Khmelenina, Valentina N. FEMS Microbiology Letters, Vol. 288, Issue 2 https://doi.org/10.1111/j.1574-6968.2008.01366.x	journal	November 2008
Identification of malic and soluble oxaloacetate decarboxylase enzymes in Enterococcus faecalis Espariz, Martín; Repizo, Guillermo; Blancato, Víctor FEBS Journal, Vol. 278, Issue 12 https://doi.org/10.1111/j.1742-4658.2011.08131.x	journal	May 2011
Reassessment of the Transhydrogenase/Malate Shunt Pathway in Clostridium thermocellum ATCC 27405 through Kinetic Characterization of Malic Enzyme and Malate Dehydrogenase Taillefer, M.; Rydzak, T.; Levin, D. B. Applied and Environmental Microbiology, Vol. 81, Issue 7 https://doi.org/10.1128/AEM.03360-14	journal	January 2015
Purification and characterization of a malic enzyme from the ruminal bacterium Streptococcus bovis ATCC 15352 and cloning and sequencing of its gene Kawai, S.; Suzuki, H.; Yamamoto, K. Applied and Environmental Microbiology, Vol. 62, Issue 8 https://doi.org/10.1128/AEM.62.8.2692-2700.1996	journal	August 1996
Purification and Characterization of an NAD-Malic Enzyme from Bradyrhizobium japonicum A1017 Chen, Fan; Okabe, Youichi; Osano, Kaoru Applied and Environmental Microbiology, Vol. 64, Issue 10 https://doi.org/10.1128/AEM.64.10.4073-4075.1998	journal	October 1998
Cloning of the Malic Enzyme Gene from Corynebacterium glutamicum and Role of the Enzyme in Lactate Metabolism Gourdon, Pierre; Baucher, Marie-France; Lindley, Nic D. Applied and Environmental Microbiology, Vol. 66, Issue 7 https://doi.org/10.1128/AEM.66.7.2981-2987.2000	journal	July 2000
YtsJ Has the Major Physiological Role of the Four Paralogous Malic Enzyme Isoforms in Bacillus subtilis Lerondel, G.; Doan, T.; Zamboni, N. Journal of Bacteriology, Vol. 188, Issue 13 https://doi.org/10.1128/JB.00167-06	journal	June 2006
Escherichia coli Malic Enzymes: Two Isoforms with Substantial Differences in Kinetic Properties, Metabolic Regulation, and Structure Bologna, F. P.; Andreo, C. S.; Drincovich, M. F. Journal of Bacteriology, Vol. 189, Issue 16 https://doi.org/10.1128/JB.00428-07	journal	June 2007
Genome Sequence of the Haloalkaliphilic Methanotrophic Bacterium Methylomicrobium alcaliphilum 20Z Vuilleumier, S.; Khmelenina, V. N.; Bringel, F. Journal of Bacteriology, Vol. 194, Issue 2 https://doi.org/10.1128/JB.06392-11	journal	December 2011
Methanotrophic bacteria. Hanson, R. S.; Hanson, T. E. Microbiological reviews, Vol. 60, Issue 2 https://doi.org/10.1128/MR.60.2.439-471.1996	journal	January 1996
Draft Genome Sequence of “Candidatus Methylacidiphilum kamchatkense” Strain Kam1, a Thermoacidophilic Methanotrophic Verrucomicrobium Erikstad, Helge-André; Birkeland, Nils-Kåre Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomeA.00065-15	journal	March 2015
Draft Genome Sequence of Methyloferula stellata AR4, an Obligate Methanotroph Possessing Only a Soluble Methane Monooxygenase Dedysh, Svetlana N.; Naumoff, Daniil G.; Vorobev, Alexey V. Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomeA.01555-14	journal	March 2015
Properties of Malic Enzyme from the Aerobic Methanotroph Methylosinus trichosporium Rozova, O. N.; Khmelenina, V. N.; Mustakhimov, I. I. Biochemistry (Moscow), Vol. 84, Issue 4 https://doi.org/10.1134/S0006297919040060	journal	April 2019
The Expanding World of Methylotrophic Metabolism Chistoserdova, Ludmila; Kalyuzhnaya, Marina G.; Lidstrom, Mary E. Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073600	journal	October 2009
The genomic landscape of the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV Anvar, Seyed; Frank, Jeroen; Pol, Arjan BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-914	journal	January 2014
Loss of malic enzymes leads to metabolic imbalance and altered levels of trehalose and putrescine in the bacterium Sinorhizobium meliloti Zhang, Ye; Smallbone, Laura Anne; diCenzo, George C. BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0780-x	journal	July 2016
Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1) de la Torre, Andrea; Metivier, Aisha; Chu, Frances Microbial Cell Factories, Vol. 14, Issue 1 https://doi.org/10.1186/s12934-015-0377-3	journal	November 2015
Purification and Characterization of the NADP-Malic Enzyme fromBradyrhizobium japonicumA1017 Chen, Fan; Okabe, Youichi; Osano, Kaoru Bioscience, Biotechnology, and Biochemistry, Vol. 61, Issue 2 https://doi.org/10.1271/bbb.61.384	journal	January 1997
Wide Distribution of Genes for Tetrahydromethanopterin/Methanofuran-Linked C1 Transfer Reactions Argues for Their Presence in the Common Ancestor of Bacteria and Archaea Chistoserdova, Ludmila Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01425	journal	September 2016
Role of NAD+-Dependent Malate Dehydrogenase in the Metabolism of Methylomicrobium alcaliphilum 20Z and Methylosinus trichosporium OB3b Rozova, Olga; Khmelenina, Valentina; Bocharova, Ksenia Microorganisms, Vol. 3, Issue 1 https://doi.org/10.3390/microorganisms3010047	journal	February 2015
Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1) [Supplemental Data] Torre, Andrea; Metivier, Aisha; Chu, Frances figshare-Supplementary information for journal article at DOI: 10.1186/s12934-015-0377-3, 3 files https://doi.org/10.6084/m9.figshare.c.3598565	collection	November 2015
Loss of malic enzymes leads to metabolic imbalance and altered levels of trehalose and putrescine in the bacterium Sinorhizobium meliloti Zhang, Ye; Smallbone, Laura; diCenzo, George figshare https://doi.org/10.6084/m9.figshare.c.3607925	collection	January 2016

Cited By (1)

Ectoine degradation pathway in halotolerant methylotrophs Reshetnikov, Aleksander S.; Rozova, Olga N.; Trotsenko, Yuri A. PLOS ONE, Vol. 15, Issue 4 https://doi.org/10.1371/journal.pone.0232244	journal	April 2020

Similar Records

Optimization of electroporation method and promoter evaluation for type-1 methanotroph, Methylotuvimicrobium alcaliphilum

Journal Article · 2024 · Frontiers in Bioengineering and Biotechnology · OSTI ID:2350870

Goswami, Shubhasish; Singer, Steven W.; Simmons, Blake A.; +1 more

Methane utilization in Methylomicrobium alcaliphilum 20Z^R: a systems approach

Journal Article · 2018 · Scientific Reports · OSTI ID:1422031

Akberdin, Ilya R.; Thompson, Merlin; Hamilton, Richard; +5 more

Kinetic and isotope partitioning studies on the NAD/sup +/-malic enzyme from Ascaris suum. [/sup 14/C tracer techniques]

Journal Article · 1978 · J. Biol. Chem.; (United States) · OSTI ID:6654839

Landsperger, W J; Fodge, D W; Harris, B G

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Role of the malic enzyme in metabolism of the halotolerant methanotroph Methylotuvimicrobium alcaliphilum 20Z

Citation Formats

References (94)

Cited By (1)

Similar Records

Related Subjects