Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea

Nayak, Dipti D.; Mahanta, Nilkamal; Mitchell, Douglas A.; Metcalf, William W.

doi:10.7554/eLife.29218

Title: Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea

Journal Article · Thu Sep 07 00:00:00 EDT 2017 · eLife

DOI:https://doi.org/10.7554/eLife.29218· OSTI ID:1378144

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Univ. of Illinois at Urbana-Champaign, IL (United States). Carl R. Woese Inst. for Genomic Biology
Univ. of Illinois at Urbana-Champaign, IL (United States). Dept. of Chemistry
Univ. of Illinois at Urbana-Champaign, IL (United States). Carl R. Woese Inst. for Genomic Biology and Dept. of Chemistry and Dept. of Microbiology
Univ. of Illinois at Urbana-Champaign, IL (United States). Carl R. Woese Inst. for Genomic Biology and Dept. of Microbiology

Methyl-coenzyme M reductase (MCR), found in strictly anaerobic methanogenic and methanotrophic archaea, catalyzes the reversible production and consumption of the potent greenhouse gas methane. The α subunit of MCR (McrA) contains several unusual post-translational modifications, including a rare thioamidation of glycine. Based on the presumed function of homologous genes involved in the biosynthesis of thioviridamide, a thioamide-containing natural product, we hypothesized that the archaeal tfuA and ycaO genes would be responsible for post-translational installation of thioglycine into McrA. Mass spectrometric characterization of McrA from the methanogenic archaeon Methanosarcina acetivorans lacking tfuA and/or ycaO revealed the presence of glycine, rather than thioglycine, supporting this hypothesis. Phenotypic characterization of the ΔycaO-tfuA mutant revealed a severe growth rate defect on substrates with low free energy yields and at elevated temperatures (39°C - 45°C). Thus, our analyses support a role for thioglycine in stabilizing the protein secondary structure near the active site.

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Research Organization:: Univ. of Illinois at Urbana-Champaign, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; National Institutes of Health (NIH); Simons Foundation; Life Sciences Research Foundation (LSRF)

Grant/Contract Number:: FG02-02ER15296; GM097142

OSTI ID:: 1378144

Alternate ID(s):: OSTI ID: 1378147; OSTI ID: 1429098; OSTI ID: 1595337

Journal Information:: eLife, Journal Name: eLife Vol. 6; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

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References (66)

Biosynthesis of the Antimetabolite 6-Thioguanine in Erwinia amylovora Plays a Key Role in Fire Blight Pathogenesis Coyne, Sébastien; Chizzali, Cornelia; Khalil, Mohammed N. A. Angewandte Chemie International Edition, Vol. 52, Issue 40 https://doi.org/10.1002/anie.201305595	journal	August 2013
YcaO domains use ATP to activate amide backbones during peptide cyclodehydrations Dunbar, Kyle L.; Melby, Joel O.; Mitchell, Douglas A. Nature Chemical Biology, Vol. 8, Issue 6 https://doi.org/10.1038/nchembio.944	journal	April 2012
The Biosynthesis of Methylated Amino Acids in the Active Site Region of Methyl-coenzyme M Reductase Selmer, Thorsten; Kahnt, Jörg; Goubeaud, Marcel Journal of Biological Chemistry, Vol. 275, Issue 6 https://doi.org/10.1074/jbc.275.6.3755	journal	February 2000
Cloning and Heterologous Expression of the Thioviridamide Biosynthesis Gene Cluster from Streptomyces olivoviridis Izawa, Masumi; Kawasaki, Takashi; Hayakawa, Yoichi Applied and Environmental Microbiology, Vol. 79, Issue 22 https://doi.org/10.1128/AEM.01978-13	journal	August 2013
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data Kearse, M.; Moir, R.; Wilson, A. Bioinformatics, Vol. 28, Issue 12 https://doi.org/10.1093/bioinformatics/bts199	journal	April 2012
The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological Diversity Galagan, J. E. Genome Research, Vol. 12, Issue 4 https://doi.org/10.1101/gr.223902	journal	April 2002
Sch 18640. A new thiostrepton-type antibiotic Puar, M. S.; Ganguly, A. K.; Afonso, A. Journal of the American Chemical Society, Vol. 103, Issue 17 https://doi.org/10.1021/ja00407a047	journal	August 1981
Two genetically distinct methyl-coenzyme M reductases in Methanobacterium thermoautotrophicum strain Marburg and DeltaH Rospert, Sabine; Linder, Dietmar; Ellermann, Joachim European Journal of Biochemistry, Vol. 194, Issue 3 https://doi.org/10.1111/j.1432-1033.1990.tb19481.x	journal	December 1990
Post-translational modifications in the active site region of methyl-coenzyme M reductase from methanogenic and methanotrophic archaea: Methanogenic archaea methyl-coenzyme M reductase Kahnt, Jörg; Buchenau, Bärbel; Mahlert, Felix FEBS Journal, Vol. 274, Issue 18 https://doi.org/10.1111/j.1742-4658.2007.06016.x	journal	August 2007
Bacterial gene import and mesophilic adaptation in archaea López-García, Purificación; Zivanovic, Yvan; Deschamps, Philippe Nature Reviews Microbiology, Vol. 13, Issue 7 https://doi.org/10.1038/nrmicro3485	journal	June 2015
Genetic Analysis of the Methanol- and Methylamine-Specific Methyltransferase 2 Genes of Methanosarcina acetivorans C2A Bose, A.; Pritchett, M. A.; Metcalf, W. W. Journal of Bacteriology, Vol. 190, Issue 11 https://doi.org/10.1128/JB.00117-08	journal	March 2008
A Methanogenic Archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov. Franzmann, P. D.; Springer, N.; Ludwig, W. Systematic and Applied Microbiology, Vol. 15, Issue 4 https://doi.org/10.1016/S0723-2020(11)80117-7	journal	December 1992
Discovery of a new ATP-binding motif involved in peptidic azoline biosynthesis Dunbar, Kyle L.; Chekan, Jonathan R.; Cox, Courtney L. Nature Chemical Biology, Vol. 10, Issue 10 https://doi.org/10.1038/nchembio.1608	journal	August 2014
Elucidation of the biosynthesis of the methane catalyst coenzyme F430 Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher Nature, Vol. 543, Issue 7643 https://doi.org/10.1038/nature21427	journal	February 2017
Methanol-Dependent Gene Expression Demonstrates that Methyl-Coenzyme M Reductase Is Essential in Methanosarcina acetivorans C2A and Allows Isolation of Mutants with Defects in Regulation of the Methanol Utilization Pathway Rother, M.; Boccazzi, P.; Bose, A. Journal of Bacteriology, Vol. 187, Issue 16 https://doi.org/10.1128/JB.187.16.5552-5559.2005	journal	August 2005
Evidence That ThiI, an Enzyme Shared between Thiamin and 4-Thiouridine Biosynthesis, May Be a Sulfurtransferase That Proceeds through a Persulfide Intermediate Palenchar, Peter M.; Buck, Christopher J.; Cheng, Hui Journal of Biological Chemistry, Vol. 275, Issue 12 https://doi.org/10.1074/jbc.275.12.8283	journal	March 2000
Comparison of three methyl-coenzyme M reductases from phylogenetically distant organisms: unusual amino acid modification, conservation and adaptation Grabarse, Wolfgang; Mahlert, Felix; Shima, Seigo Journal of Molecular Biology, Vol. 303, Issue 2 https://doi.org/10.1006/jmbi.2000.4136	journal	October 2000
IscS Functions as a Primary Sulfur-donating Enzyme by Interacting Specifically with MoeB and MoaD in the Biosynthesis of Molybdopterin in Escherichia coli Zhang, Wanjiao; Urban, Alexander; Mihara, Hisaaki Journal of Biological Chemistry, Vol. 285, Issue 4 https://doi.org/10.1074/jbc.M109.082172	journal	November 2009
Genome mining for methanobactins Kenney, Grace E.; Rosenzweig, Amy C. BMC Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1741-7007-11-17	journal	February 2013
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria Kim, H. J. Science, Vol. 305, Issue 5690 https://doi.org/10.1126/science.1098322	journal	September 2004
Molybdenum Cofactor Biosynthesis in Humans: Identification of a Persulfide Group in the Rhodanese-like Domain of MOCS3 by Mass Spectrometry ^† Matthies, Andreas; Nimtz, Manfred; Leimkühler, Silke Biochemistry, Vol. 44, Issue 21 https://doi.org/10.1021/bi0503448	journal	May 2005
Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways Schulman, Brenda A.; Wade Harper, J. Nature Reviews Molecular Cell Biology, Vol. 10, Issue 5 https://doi.org/10.1038/nrm2673	journal	April 2009
Identification of an Auxiliary Leader Peptide-Binding Protein Required for Azoline Formation in Ribosomal Natural Products Dunbar, Kyle L.; Tietz, Jonathan I.; Cox, Courtney L. Journal of the American Chemical Society, Vol. 137, Issue 24 https://doi.org/10.1021/jacs.5b04682	journal	June 2015
The radical mechanism of biological methane synthesis by methyl-coenzyme M reductase Wongnate, T.; Sliwa, D.; Ginovska, B. Science, Vol. 352, Issue 6288 https://doi.org/10.1126/science.aaf0616	journal	May 2016
Purified Methyl-Coenzyme-M Reductase is Activated when the Enzyme-Bound Coenzyme F430 is Reduced to the Nickel(I) Oxidation State by Titanium(III) Citrate Goubeaud, Marcel; Schreiner, Guido; Thauer, Rudolf K. European Journal of Biochemistry, Vol. 243, Issue 1-2 https://doi.org/10.1111/j.1432-1033.1997.00110.x	journal	January 1997
Different Biosynthetic Pathways to Fosfomycin in Pseudomonas syringae and Streptomyces Species Kim, Seung Young; Ju, Kou-San; Metcalf, William W. Antimicrobial Agents and Chemotherapy, Vol. 56, Issue 8 https://doi.org/10.1128/AAC.06478-11	journal	May 2012
On the mechanism of biological methane formation: structural evidence for conformational changes in methyl-coenzyme M reductase upon substrate binding Grabarse, Wolfgang; Mahlert, Felix; Duin, Evert C. Journal of Molecular Biology, Vol. 309, Issue 1 https://doi.org/10.1006/jmbi.2001.4647	journal	May 2001
Protein splicing and autoproteolysis mechanisms Perler, Francine B.; Xu, Ming-Qun; Paulus, Henry Current Opinion in Chemical Biology, Vol. 1, Issue 3 https://doi.org/10.1016/S1367-5931(97)80065-8	journal	October 1997
Chemistry and Biology of the Copper Chelator Methanobactin Kenney, Grace E.; Rosenzweig, Amy C. ACS Chemical Biology, Vol. 7, Issue 2 https://doi.org/10.1021/cb2003913	journal	November 2011
Structure of Thioviridamide, a Novel Apoptosis Inducer from Streptomyces olivoviridis Hayakawa, Yoichi; Sasaki, Kahori; Nagai, Koji The Journal of Antibiotics, Vol. 59, Issue 1 https://doi.org/10.1038/ja.2006.2	journal	January 2006
Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity Sowers, Kevin R.; Boone, Jane E.; Gunsalus, Robert P. Applied and Environmental Microbiology, Vol. 59, Issue 11 https://doi.org/10.1128/AEM.59.11.3832-3839.1993	journal	January 1993
Hydrogen Bonding Abilities of Thioamide Lee, Ho-Jin; Choi, Young-Sang; Lee, Kang-Bong The Journal of Physical Chemistry A, Vol. 106, Issue 30 https://doi.org/10.1021/jp025516e	journal	August 2002
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L. Science, Vol. 354, Issue 6310 https://doi.org/10.1126/science.aag2947	journal	October 2016
A prevalent peptide-binding domain guides ribosomal natural product biosynthesis Burkhart, Brandon J.; Hudson, Graham A.; Dunbar, Kyle L. Nature Chemical Biology, Vol. 11, Issue 8 https://doi.org/10.1038/nchembio.1856	journal	July 2015
An Anaerobic, Intrachamber Incubator for Growth ofMethanosarcina spp. on Methanol-Containing Solid Media Metcalf, William W.; Zhang, Jun Kai; Wolfe, Ralph S. Applied and Environmental Microbiology, Vol. 64, Issue 2 https://doi.org/10.1128/AEM.64.2.768-770.1998	journal	January 1998
Closthioamide: An Unprecedented Polythioamide Antibiotic from the Strictly Anaerobic Bacterium Clostridium cellulolyticum Lincke, Thorger; Behnken, Swantje; Ishida, Keishi Angewandte Chemie, Vol. 122, Issue 11 https://doi.org/10.1002/ange.200906114	journal	February 2010
In-gel digestion for mass spectrometric characterization of proteins and proteomes Shevchenko, Andrej; Tomas, Henrik; Havli, Jan Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.468	journal	December 2006
Novel reactions involved in energy conservation by methanogenic archaea Deppenmeier, Uwe; Lienard, Tanja; Gottschalk, Gerhard FEBS Letters, Vol. 457, Issue 3 https://doi.org/10.1016/S0014-5793(99)01026-1	journal	September 1999
A genetic system for Archaea of the genus Methanosarcina: Liposome-mediated transformation and construction of shuttle vectors Metcalf, W. W.; Zhang, J. K.; Apolinario, E. Proceedings of the National Academy of Sciences, Vol. 94, Issue 6 https://doi.org/10.1073/pnas.94.6.2626	journal	March 1997
Nonprotein amino acids from Cycas revoluta Pan, Meide; Mabry, Tom J.; Beale, John M. Phytochemistry, Vol. 45, Issue 3 https://doi.org/10.1016/S0031-9422(96)00866-7	journal	June 1997
Total structure of the highly modified peptide antibiotic components of thiopeptin. Hensens, Otto D.; Albers-SchÖNberg, Georg The Journal of Antibiotics, Vol. 36, Issue 7 https://doi.org/10.7164/antibiotics.36.814	journal	January 1983
The physiology and habitat of the last universal common ancestor Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia Nature Microbiology, Vol. 1, Issue 9 https://doi.org/10.1038/nmicrobiol.2016.116	journal	July 2016
Genetic Basis for Metabolism of Methylated Sulfur Compounds in Methanosarcina Species Fu, He; Metcalf, William W. Journal of Bacteriology, Vol. 197, Issue 8 https://doi.org/10.1128/JB.02605-14	journal	February 2015
Biosynthesis of the Thiazole Moiety of Thiamin Pyrophosphate (Vitamin B1) ^† Park, Joo-Heon; Dorrestein, Pieter C.; Zhai, Huili Biochemistry, Vol. 42, Issue 42 https://doi.org/10.1021/bi034902z	journal	October 2003
Molecular, genetic, and biochemical characterization of the serC gene of Methanosarcina barkeri Fusaro. Metcalf, W. W.; Zhang, J. K.; Shi, X. Journal of Bacteriology, Vol. 178, Issue 19 https://doi.org/10.1128/jb.178.19.5797-5802.1996	journal	October 1996
Mode of action of closthioamide: the first member of the polythioamide class of bacterial DNA gyrase inhibitors Chiriac, Alina Iulia; Kloss, Florian; Krämer, Jonas Journal of Antimicrobial Chemotherapy, Vol. 70, Issue 9 https://doi.org/10.1093/jac/dkv161	journal	July 2015
Crystal Structure of Methyl-Coenzyme M Reductase: The Key Enzyme of Biological Methane Formation Ermler, U. Science, Vol. 278, Issue 5342 https://doi.org/10.1126/science.278.5342.1457	journal	November 1997
ProPhylo: partial phylogenetic profiling to guide protein family construction and assignment of biological process Basu, Malay K.; Selengut, Jeremy D.; Haft, Daniel H. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-434	journal	November 2011
The origin and evolution of Archaea: a state of the art Gribaldo, Simonetta; Brochier-Armanet, Celine Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1470 https://doi.org/10.1098/rstb.2006.1841	journal	May 2006
The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane Scheller, Silvan; Goenrich, Meike; Boecher, Reinhard Nature, Vol. 465, Issue 7298 https://doi.org/10.1038/nature09015	journal	June 2010
Direct evidence for enzyme persulfide and disulfide intermediates during 4-thiouridine biosynthesis Wright, Chapman M.; Christman, Glenn D.; Snellinger, Ann M. Chemical Communications, Issue 29 https://doi.org/10.1039/b604040c	journal	January 2006
Methanogenic archaea: ecologically relevant differences in energy conservation Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning Nature Reviews Microbiology, Vol. 6, Issue 8 https://doi.org/10.1038/nrmicro1931	journal	June 2008
Didehydroaspartate Modification in Methyl-Coenzyme M Reductase Catalyzing Methane Formation Wagner, Tristan; Kahnt, Jörg; Ermler, Ulrich Angewandte Chemie International Edition, Vol. 55, Issue 36 https://doi.org/10.1002/anie.201603882	journal	July 2016
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H. Nature Microbiology, Vol. 1, Issue 12 https://doi.org/10.1038/nmicrobiol.2016.170	journal	October 2016
YcaO-Dependent Posttranslational Amide Activation: Biosynthesis, Structure, and Function Burkhart, Brandon J.; Schwalen, Christopher J.; Mann, Greg Chemical Reviews, Vol. 117, Issue 8 https://doi.org/10.1021/acs.chemrev.6b00623	journal	March 2017
Mechanistic Studies of Methane Biogenesis by Methyl-Coenzyme M Reductase: Evidence that Coenzyme B Participates in Cleaving the C−S Bond of Methyl-Coenzyme M ^† Horng, Yih-Chern; Becker, Donald F.; Ragsdale, Stephen W. Biochemistry, Vol. 40, Issue 43 https://doi.org/10.1021/bi011196y	journal	October 2001
The universal tree of life: an update Forterre, Patrick Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00717	journal	July 2015
Control of Plant Defense Mechanisms and Fire Blight Pathogenesis through the Regulation of 6-Thioguanine Biosynthesis in Erwinia amylovora Coyne, Sébastien; Litomska, Agnieszka; Chizzali, Cornelia ChemBioChem, Vol. 15, Issue 3 https://doi.org/10.1002/cbic.201300684	journal	January 2014
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
Why Does Thioformamide Have a Larger Rotational Barrier Than Formamide? Wiberg, Kenneth B.; Rablen, Paul R. Journal of the American Chemical Society, Vol. 117, Issue 8 https://doi.org/10.1021/ja00113a009	journal	March 1995
On the use of thioamides as fluorescence quenching probes for tracking protein folding and stability Petersson, E. James; Goldberg, Jacob M.; Wissner, Rebecca F. Phys. Chem. Chem. Phys., Vol. 16, Issue 15 https://doi.org/10.1039/C3CP55525A	journal	January 2014
Phylogenomic Data Support a Seventh Order of Methylotrophic Methanogens and Provide Insights into the Evolution of Methanogenesis Borrel, Guillaume; O’Toole, Paul W.; Harris, Hugh M. B. Genome Biology and Evolution, Vol. 5, Issue 10 https://doi.org/10.1093/gbe/evt128	journal	August 2013
Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans Nayak, Dipti D.; Metcalf, William W. Proceedings of the National Academy of Sciences, Vol. 114, Issue 11 https://doi.org/10.1073/pnas.1618596114	journal	March 2017
Analysis of Protein Stability and Ligand Interactions by Thermal Shift Assay Huynh, Kathy; Partch, Carrie L. Current Protocols in Protein Science, Vol. 79, Issue 1 https://doi.org/10.1002/0471140864.ps2809s79	journal	February 2015
New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species Guss, Adam M.; Rother, Michael; Zhang, Jun Kai Archaea, Vol. 2, Issue 3 https://doi.org/10.1155/2008/534081	journal	January 2008
Temperature dependence of methyl-coenzyme M reductase activity and of the formation of the methyl-coenzyme M reductase red2 state induced by coenzyme B Goenrich, Meike; Duin, Evert C.; Mahlert, Felix JBIC Journal of Biological Inorganic Chemistry, Vol. 10, Issue 4 https://doi.org/10.1007/s00775-005-0636-6	journal	April 2005

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