Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea
Abstract
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.
- Authors:
-
- 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
- Publication Date:
- Research Org.:
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- Sponsoring Org.:
- 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)
- OSTI Identifier:
- 1378144
- Alternate Identifier(s):
- OSTI ID: 1378147; OSTI ID: 1429098; OSTI ID: 1595337
- Grant/Contract Number:
- FG02-02ER15296; GM097142
- Resource Type:
- Published Article
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Name: eLife Journal Volume: 6; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; 03 NATURAL GAS
Citation Formats
Nayak, Dipti D., Mahanta, Nilkamal, Mitchell, Douglas A., and Metcalf, William W. Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea. United States: N. p., 2017.
Web. doi:10.7554/eLife.29218.
Nayak, Dipti D., Mahanta, Nilkamal, Mitchell, Douglas A., & Metcalf, William W. Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea. United States. https://doi.org/10.7554/eLife.29218
Nayak, Dipti D., Mahanta, Nilkamal, Mitchell, Douglas A., and Metcalf, William W. Thu .
"Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea". United States. https://doi.org/10.7554/eLife.29218.
@article{osti_1378144,
title = {Post-translational thioamidation of methyl-coenzyme M reductase, a key enzyme in methanogenic and methanotrophic Archaea},
author = {Nayak, Dipti D. and Mahanta, Nilkamal and Mitchell, Douglas A. and Metcalf, William W.},
abstractNote = {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.},
doi = {10.7554/eLife.29218},
journal = {eLife},
number = ,
volume = 6,
place = {United States},
year = {Thu Sep 07 00:00:00 EDT 2017},
month = {Thu Sep 07 00:00:00 EDT 2017}
}
https://doi.org/10.7554/eLife.29218
Web of Science
Works referenced in this record:
Biosynthesis of the Antimetabolite 6-Thioguanine in Erwinia amylovora Plays a Key Role in Fire Blight Pathogenesis
journal, August 2013
- Coyne, Sébastien; Chizzali, Cornelia; Khalil, Mohammed N. A.
- Angewandte Chemie International Edition, Vol. 52, Issue 40
YcaO domains use ATP to activate amide backbones during peptide cyclodehydrations
journal, April 2012
- Dunbar, Kyle L.; Melby, Joel O.; Mitchell, Douglas A.
- Nature Chemical Biology, Vol. 8, Issue 6
The Biosynthesis of Methylated Amino Acids in the Active Site Region of Methyl-coenzyme M Reductase
journal, February 2000
- Selmer, Thorsten; Kahnt, Jörg; Goubeaud, Marcel
- Journal of Biological Chemistry, Vol. 275, Issue 6
Cloning and Heterologous Expression of the Thioviridamide Biosynthesis Gene Cluster from Streptomyces olivoviridis
journal, August 2013
- Izawa, Masumi; Kawasaki, Takashi; Hayakawa, Yoichi
- Applied and Environmental Microbiology, Vol. 79, Issue 22
Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data
journal, April 2012
- Kearse, M.; Moir, R.; Wilson, A.
- Bioinformatics, Vol. 28, Issue 12
The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological Diversity
journal, April 2002
- Galagan, J. E.
- Genome Research, Vol. 12, Issue 4
Sch 18640. A new thiostrepton-type antibiotic
journal, August 1981
- Puar, M. S.; Ganguly, A. K.; Afonso, A.
- Journal of the American Chemical Society, Vol. 103, Issue 17
Two genetically distinct methyl-coenzyme M reductases in Methanobacterium thermoautotrophicum strain Marburg and DeltaH
journal, December 1990
- Rospert, Sabine; Linder, Dietmar; Ellermann, Joachim
- European Journal of Biochemistry, Vol. 194, Issue 3
Post-translational modifications in the active site region of methyl-coenzyme M reductase from methanogenic and methanotrophic archaea: Methanogenic archaea methyl-coenzyme M reductase
journal, August 2007
- Kahnt, Jörg; Buchenau, Bärbel; Mahlert, Felix
- FEBS Journal, Vol. 274, Issue 18
Bacterial gene import and mesophilic adaptation in archaea
journal, June 2015
- López-García, Purificación; Zivanovic, Yvan; Deschamps, Philippe
- Nature Reviews Microbiology, Vol. 13, Issue 7
Genetic Analysis of the Methanol- and Methylamine-Specific Methyltransferase 2 Genes of Methanosarcina acetivorans C2A
journal, March 2008
- Bose, A.; Pritchett, M. A.; Metcalf, W. W.
- Journal of Bacteriology, Vol. 190, Issue 11
A Methanogenic Archaeon from Ace Lake, Antarctica: Methanococcoides burtonii sp. nov.
journal, December 1992
- Franzmann, P. D.; Springer, N.; Ludwig, W.
- Systematic and Applied Microbiology, Vol. 15, Issue 4
Discovery of a new ATP-binding motif involved in peptidic azoline biosynthesis
journal, August 2014
- Dunbar, Kyle L.; Chekan, Jonathan R.; Cox, Courtney L.
- Nature Chemical Biology, Vol. 10, Issue 10
Elucidation of the biosynthesis of the methane catalyst coenzyme F430
journal, February 2017
- Moore, Simon J.; Sowa, Sven T.; Schuchardt, Christopher
- Nature, Vol. 543, Issue 7643
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
journal, August 2005
- Rother, M.; Boccazzi, P.; Bose, A.
- Journal of Bacteriology, Vol. 187, Issue 16
Evidence That ThiI, an Enzyme Shared between Thiamin and 4-Thiouridine Biosynthesis, May Be a Sulfurtransferase That Proceeds through a Persulfide Intermediate
journal, March 2000
- Palenchar, Peter M.; Buck, Christopher J.; Cheng, Hui
- Journal of Biological Chemistry, Vol. 275, Issue 12
Comparison of three methyl-coenzyme M reductases from phylogenetically distant organisms: unusual amino acid modification, conservation and adaptation
journal, October 2000
- Grabarse, Wolfgang; Mahlert, Felix; Shima, Seigo
- Journal of Molecular Biology, Vol. 303, Issue 2
IscS Functions as a Primary Sulfur-donating Enzyme by Interacting Specifically with MoeB and MoaD in the Biosynthesis of Molybdopterin in Escherichia coli
journal, November 2009
- Zhang, Wanjiao; Urban, Alexander; Mihara, Hisaaki
- Journal of Biological Chemistry, Vol. 285, Issue 4
Genome mining for methanobactins
journal, February 2013
- Kenney, Grace E.; Rosenzweig, Amy C.
- BMC Biology, Vol. 11, Issue 1
Methanobactin, a Copper-Acquisition Compound from Methane-Oxidizing Bacteria
journal, September 2004
- Kim, H. J.
- Science, Vol. 305, Issue 5690
Molybdenum Cofactor Biosynthesis in Humans: Identification of a Persulfide Group in the Rhodanese-like Domain of MOCS3 by Mass Spectrometry †
journal, May 2005
- Matthies, Andreas; Nimtz, Manfred; Leimkühler, Silke
- Biochemistry, Vol. 44, Issue 21
Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways
journal, April 2009
- Schulman, Brenda A.; Wade Harper, J.
- Nature Reviews Molecular Cell Biology, Vol. 10, Issue 5
Identification of an Auxiliary Leader Peptide-Binding Protein Required for Azoline Formation in Ribosomal Natural Products
journal, June 2015
- Dunbar, Kyle L.; Tietz, Jonathan I.; Cox, Courtney L.
- Journal of the American Chemical Society, Vol. 137, Issue 24
The radical mechanism of biological methane synthesis by methyl-coenzyme M reductase
journal, May 2016
- Wongnate, T.; Sliwa, D.; Ginovska, B.
- Science, Vol. 352, Issue 6288
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
journal, January 1997
- Goubeaud, Marcel; Schreiner, Guido; Thauer, Rudolf K.
- European Journal of Biochemistry, Vol. 243, Issue 1-2
Different Biosynthetic Pathways to Fosfomycin in Pseudomonas syringae and Streptomyces Species
journal, May 2012
- Kim, Seung Young; Ju, Kou-San; Metcalf, William W.
- Antimicrobial Agents and Chemotherapy, Vol. 56, Issue 8
On the mechanism of biological methane formation: structural evidence for conformational changes in methyl-coenzyme M reductase upon substrate binding
journal, May 2001
- Grabarse, Wolfgang; Mahlert, Felix; Duin, Evert C.
- Journal of Molecular Biology, Vol. 309, Issue 1
Protein splicing and autoproteolysis mechanisms
journal, October 1997
- Perler, Francine B.; Xu, Ming-Qun; Paulus, Henry
- Current Opinion in Chemical Biology, Vol. 1, Issue 3
Chemistry and Biology of the Copper Chelator Methanobactin
journal, November 2011
- Kenney, Grace E.; Rosenzweig, Amy C.
- ACS Chemical Biology, Vol. 7, Issue 2
Structure of Thioviridamide, a Novel Apoptosis Inducer from Streptomyces olivoviridis
journal, January 2006
- Hayakawa, Yoichi; Sasaki, Kahori; Nagai, Koji
- The Journal of Antibiotics, Vol. 59, Issue 1
Disaggregation of Methanosarcina spp. and Growth as Single Cells at Elevated Osmolarity
journal, January 1993
- Sowers, Kevin R.; Boone, Jane E.; Gunsalus, Robert P.
- Applied and Environmental Microbiology, Vol. 59, Issue 11
Hydrogen Bonding Abilities of Thioamide
journal, August 2002
- Lee, Ho-Jin; Choi, Young-Sang; Lee, Kang-Bong
- The Journal of Physical Chemistry A, Vol. 106, Issue 30
The biosynthetic pathway of coenzyme F430 in methanogenic and methanotrophic archaea
journal, October 2016
- Zheng, Kaiyuan; Ngo, Phong D.; Owens, Victoria L.
- Science, Vol. 354, Issue 6310
A prevalent peptide-binding domain guides ribosomal natural product biosynthesis
journal, July 2015
- Burkhart, Brandon J.; Hudson, Graham A.; Dunbar, Kyle L.
- Nature Chemical Biology, Vol. 11, Issue 8
An Anaerobic, Intrachamber Incubator for Growth ofMethanosarcina spp. on Methanol-Containing Solid Media
journal, January 1998
- Metcalf, William W.; Zhang, Jun Kai; Wolfe, Ralph S.
- Applied and Environmental Microbiology, Vol. 64, Issue 2
Closthioamide: An Unprecedented Polythioamide Antibiotic from the Strictly Anaerobic Bacterium Clostridium cellulolyticum
journal, February 2010
- Lincke, Thorger; Behnken, Swantje; Ishida, Keishi
- Angewandte Chemie, Vol. 122, Issue 11
In-gel digestion for mass spectrometric characterization of proteins and proteomes
journal, December 2006
- Shevchenko, Andrej; Tomas, Henrik; Havli, Jan
- Nature Protocols, Vol. 1, Issue 6
Novel reactions involved in energy conservation by methanogenic archaea
journal, September 1999
- Deppenmeier, Uwe; Lienard, Tanja; Gottschalk, Gerhard
- FEBS Letters, Vol. 457, Issue 3
A genetic system for Archaea of the genus Methanosarcina: Liposome-mediated transformation and construction of shuttle vectors
journal, March 1997
- Metcalf, W. W.; Zhang, J. K.; Apolinario, E.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 6
Nonprotein amino acids from Cycas revoluta
journal, June 1997
- Pan, Meide; Mabry, Tom J.; Beale, John M.
- Phytochemistry, Vol. 45, Issue 3
Total structure of the highly modified peptide antibiotic components of thiopeptin.
journal, January 1983
- Hensens, Otto D.; Albers-SchÖNberg, Georg
- The Journal of Antibiotics, Vol. 36, Issue 7
The physiology and habitat of the last universal common ancestor
journal, July 2016
- Weiss, Madeline C.; Sousa, Filipa L.; Mrnjavac, Natalia
- Nature Microbiology, Vol. 1, Issue 9
Genetic Basis for Metabolism of Methylated Sulfur Compounds in Methanosarcina Species
journal, February 2015
- Fu, He; Metcalf, William W.
- Journal of Bacteriology, Vol. 197, Issue 8
Biosynthesis of the Thiazole Moiety of Thiamin Pyrophosphate (Vitamin B1) †
journal, October 2003
- Park, Joo-Heon; Dorrestein, Pieter C.; Zhai, Huili
- Biochemistry, Vol. 42, Issue 42
Molecular, genetic, and biochemical characterization of the serC gene of Methanosarcina barkeri Fusaro.
journal, October 1996
- Metcalf, W. W.; Zhang, J. K.; Shi, X.
- Journal of Bacteriology, Vol. 178, Issue 19
Mode of action of closthioamide: the first member of the polythioamide class of bacterial DNA gyrase inhibitors
journal, July 2015
- Chiriac, Alina Iulia; Kloss, Florian; Krämer, Jonas
- Journal of Antimicrobial Chemotherapy, Vol. 70, Issue 9
Crystal Structure of Methyl-Coenzyme M Reductase: The Key Enzyme of Biological Methane Formation
journal, November 1997
- Ermler, U.
- Science, Vol. 278, Issue 5342
ProPhylo: partial phylogenetic profiling to guide protein family construction and assignment of biological process
journal, November 2011
- Basu, Malay K.; Selengut, Jeremy D.; Haft, Daniel H.
- BMC Bioinformatics, Vol. 12, Issue 1
The origin and evolution of Archaea: a state of the art
journal, May 2006
- Gribaldo, Simonetta; Brochier-Armanet, Celine
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 361, Issue 1470
The key nickel enzyme of methanogenesis catalyses the anaerobic oxidation of methane
journal, June 2010
- Scheller, Silvan; Goenrich, Meike; Boecher, Reinhard
- Nature, Vol. 465, Issue 7298
Direct evidence for enzyme persulfide and disulfide intermediates during 4-thiouridine biosynthesis
journal, January 2006
- Wright, Chapman M.; Christman, Glenn D.; Snellinger, Ann M.
- Chemical Communications, Issue 29
Methanogenic archaea: ecologically relevant differences in energy conservation
journal, June 2008
- Thauer, Rudolf K.; Kaster, Anne-Kristin; Seedorf, Henning
- Nature Reviews Microbiology, Vol. 6, Issue 8
Didehydroaspartate Modification in Methyl-Coenzyme M Reductase Catalyzing Methane Formation
journal, July 2016
- Wagner, Tristan; Kahnt, Jörg; Ermler, Ulrich
- Angewandte Chemie International Edition, Vol. 55, Issue 36
Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota
journal, October 2016
- Vanwonterghem, Inka; Evans, Paul N.; Parks, Donovan H.
- Nature Microbiology, Vol. 1, Issue 12
YcaO-Dependent Posttranslational Amide Activation: Biosynthesis, Structure, and Function
journal, March 2017
- Burkhart, Brandon J.; Schwalen, Christopher J.; Mann, Greg
- Chemical Reviews, Vol. 117, Issue 8
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 †
journal, October 2001
- Horng, Yih-Chern; Becker, Donald F.; Ragsdale, Stephen W.
- Biochemistry, Vol. 40, Issue 43
The universal tree of life: an update
journal, July 2015
- Forterre, Patrick
- Frontiers in Microbiology, Vol. 6
Control of Plant Defense Mechanisms and Fire Blight Pathogenesis through the Regulation of 6-Thioguanine Biosynthesis in Erwinia amylovora
journal, January 2014
- Coyne, Sébastien; Litomska, Agnieszka; Chizzali, Cornelia
- ChemBioChem, Vol. 15, Issue 3
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Why Does Thioformamide Have a Larger Rotational Barrier Than Formamide?
journal, March 1995
- Wiberg, Kenneth B.; Rablen, Paul R.
- Journal of the American Chemical Society, Vol. 117, Issue 8
On the use of thioamides as fluorescence quenching probes for tracking protein folding and stability
journal, January 2014
- Petersson, E. James; Goldberg, Jacob M.; Wissner, Rebecca F.
- Phys. Chem. Chem. Phys., Vol. 16, Issue 15
Phylogenomic Data Support a Seventh Order of Methylotrophic Methanogens and Provide Insights into the Evolution of Methanogenesis
journal, August 2013
- Borrel, Guillaume; O’Toole, Paul W.; Harris, Hugh M. B.
- Genome Biology and Evolution, Vol. 5, Issue 10
Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans
journal, March 2017
- Nayak, Dipti D.; Metcalf, William W.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 11
Analysis of Protein Stability and Ligand Interactions by Thermal Shift Assay
journal, February 2015
- Huynh, Kathy; Partch, Carrie L.
- Current Protocols in Protein Science, Vol. 79, Issue 1
New methods for tightly regulated gene expression and highly efficient chromosomal integration of cloned genes for Methanosarcina species
journal, January 2008
- Guss, Adam M.; Rother, Michael; Zhang, Jun Kai
- Archaea, Vol. 2, Issue 3
Temperature dependence of methyl-coenzyme M reductase activity and of the formation of the methyl-coenzyme M reductase red2 state induced by coenzyme B
journal, April 2005
- Goenrich, Meike; Duin, Evert C.; Mahlert, Felix
- JBIC Journal of Biological Inorganic Chemistry, Vol. 10, Issue 4