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Title: A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase

Abstract

COG5598 comprises a large number of proteins related to MttB, the trimethylamine:corrinoid methyltransferase. MttB has a genetically encoded pyrrolysine residue proposed essential for catalysis. MttB is the only known trimethylamine methyltransferase, yet the great majority of members of COG5598 lack pyrrolysine, leaving the activity of these proteins an open question. Here, we describe the function of one of the nonpyrrolysine members of this large protein family. Three nonpyrrolysine MttB homologs are encoded in Desulfitobacterium hafniense, a Gram-positive strict anaerobe present in both the environment and human intestine. D. hafniense was found capable of growth on glycine betaine with electron acceptors such as nitrate or fumarate, producing dimethylglycine and CO 2 as products. Examination of the genome revealed genes for tetrahydrofolate-linked oxidation of a methyl group originating from a methylated corrinoid protein, but no obvious means to carry out corrinoid methylation with glycine betaine. DSY3156, encoding one of the nonpyrrolysine MttB homologs, was up-regulated during growth on glycine betaine. The recombinant DSY3156 protein converts glycine betaine and cob(I)alamin to dimethylglycine and methylcobalamin. To our knowledge, DSY3156 is the first glycine betaine:corrinoid methyltransferase described, and a designation of MtgB is proposed. Additionally, DSY3157, an adjacently encoded protein, was shown to be amore » methylcobalamin:tetrahydrofolate methyltransferase and is designated MtgA. Homologs of MtgB are widely distributed, especially in marine bacterioplankton and nitrogen-fixing plant symbionts. Lastly, they are also found in multiple members of the human microbiome, and may play a beneficial role in trimethylamine homeostasis, which in recent years has been directly tied to human cardiovascular health.« less

Authors:
 [1];  [2];  [2];  [3];  [4]
  1. Miami Univ., Oxford, OH (United States). Dept. of Microbiology
  2. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology
  3. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology and Biochemistry Program
  4. Miami Univ., Oxford, OH (United States). Dept. of Microbiology; Miami Univ., Hamilton, OH (United States)
Publication Date:
Research Org.:
The Ohio State Univ., Columbus, OH (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1348916
Grant/Contract Number:  
FG02-91ER20042
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 111; Journal Issue: 43; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; glycine betaine; trimethylamine methyltransferase; COG5598; L-pyrrolysine; Desulfitobacterium hafniense

Citation Formats

Ticak, Tomislav, Kountz, D. J., Girosky, K. E., Krzycki, J. A., and Ferguson, D. J. A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase. United States: N. p., 2014. Web. doi:10.1073/pnas.1409642111.
Ticak, Tomislav, Kountz, D. J., Girosky, K. E., Krzycki, J. A., & Ferguson, D. J. A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase. United States. doi:10.1073/pnas.1409642111.
Ticak, Tomislav, Kountz, D. J., Girosky, K. E., Krzycki, J. A., and Ferguson, D. J. Mon . "A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase". United States. doi:10.1073/pnas.1409642111. https://www.osti.gov/servlets/purl/1348916.
@article{osti_1348916,
title = {A nonpyrrolysine member of the widely distributed trimethylamine methyltransferase family is a glycine betaine methyltransferase},
author = {Ticak, Tomislav and Kountz, D. J. and Girosky, K. E. and Krzycki, J. A. and Ferguson, D. J.},
abstractNote = {COG5598 comprises a large number of proteins related to MttB, the trimethylamine:corrinoid methyltransferase. MttB has a genetically encoded pyrrolysine residue proposed essential for catalysis. MttB is the only known trimethylamine methyltransferase, yet the great majority of members of COG5598 lack pyrrolysine, leaving the activity of these proteins an open question. Here, we describe the function of one of the nonpyrrolysine members of this large protein family. Three nonpyrrolysine MttB homologs are encoded in Desulfitobacterium hafniense, a Gram-positive strict anaerobe present in both the environment and human intestine. D. hafniense was found capable of growth on glycine betaine with electron acceptors such as nitrate or fumarate, producing dimethylglycine and CO2 as products. Examination of the genome revealed genes for tetrahydrofolate-linked oxidation of a methyl group originating from a methylated corrinoid protein, but no obvious means to carry out corrinoid methylation with glycine betaine. DSY3156, encoding one of the nonpyrrolysine MttB homologs, was up-regulated during growth on glycine betaine. The recombinant DSY3156 protein converts glycine betaine and cob(I)alamin to dimethylglycine and methylcobalamin. To our knowledge, DSY3156 is the first glycine betaine:corrinoid methyltransferase described, and a designation of MtgB is proposed. Additionally, DSY3157, an adjacently encoded protein, was shown to be a methylcobalamin:tetrahydrofolate methyltransferase and is designated MtgA. Homologs of MtgB are widely distributed, especially in marine bacterioplankton and nitrogen-fixing plant symbionts. Lastly, they are also found in multiple members of the human microbiome, and may play a beneficial role in trimethylamine homeostasis, which in recent years has been directly tied to human cardiovascular health.},
doi = {10.1073/pnas.1409642111},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 43,
volume = 111,
place = {United States},
year = {2014},
month = {10}
}

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    Works referencing / citing this record:

    A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
    journal, August 2019


    Basic Local Alignment Search Tool
    journal, October 1990


    Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
    journal, December 2001


    Isolation and characterization of a tetramethylammonium-degrading Methanococcoides strain and a novel glycine betaine-utilizing Methanolobus strain
    journal, October 2014

    • Ticak, Tomislav; Hariraju, Dinesh; Arcelay, Margarette Bayron
    • Archives of Microbiology, Vol. 197, Issue 2
    • DOI: 10.1007/s00203-014-1043-6

    A Desulfitobacterium strain isolated from human feces that does not dechlorinate chloroethenes or chlorophenols
    journal, June 2001

    • van de Pas, Bram; Harmsen, Hermie; Raangs, Gerwin
    • Archives of Microbiology, Vol. 175, Issue 6
    • DOI: 10.1007/s002030100276

    Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. I. Batch cultures
    journal, November 1999

    • Keller, M. D.; Kiene, R. P.; Matrai, P. A.
    • Marine Biology, Vol. 135, Issue 2
    • DOI: 10.1007/s002270050621

    Metaproteomic Survey of Six Aquatic Habitats: Discovering the Identities of Microbial Populations Active in Biogeochemical Cycling
    journal, January 2014


    Studies of Dimethylglycine Oxidase Isoenzymes in Arthrobacter globiformis Cells
    journal, December 2010

    • Časaitė, Vida; Povilonienė, Simona; Meškienė, Rita
    • Current Microbiology, Vol. 62, Issue 4
    • DOI: 10.1007/s00284-010-9852-6

    Kinetic and structural features of betaine aldehyde dehydrogenases: Mechanistic and regulatory implications
    journal, January 2010

    • Muñoz-Clares, Rosario A.; Díaz-Sánchez, Ángel G.; González-Segura, Lilian
    • Archives of Biochemistry and Biophysics, Vol. 493, Issue 1
    • DOI: 10.1016/j.abb.2009.09.006

    Glycine reductase mechanism
    journal, October 2004


    Function of genetically encoded pyrrolysine in corrinoid-dependent methylamine methyltransferases
    journal, October 2004


    Reactivity and Chemical Synthesis of L-Pyrrolysine— the 22nd Genetically Encoded Amino Acid
    journal, September 2004


    Molecular mechanisms underlying roseobacter–phytoplankton symbioses
    journal, June 2010


    Functional context, biosynthesis, and genetic encoding of pyrrolysine
    journal, June 2011

    • Gaston, Marsha A.; Jiang, Ruisheng; Krzycki, Joseph A.
    • Current Opinion in Microbiology, Vol. 14, Issue 3
    • DOI: 10.1016/j.mib.2011.04.001

    Metabolic changes of rhizobia in legume nodules
    journal, April 2006


    Stability and Robustness of Human Metabolic Phenotypes in Response to Sequential Food Challenges
    journal, December 2011

    • Heinzmann, Silke S.; Merrifield, Claire A.; Rezzi, Serge
    • Journal of Proteome Research, Vol. 11, Issue 2
    • DOI: 10.1021/pr2005764

    Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
    journal, August 1970


    A rare SAR11 fosmid clone confirming genetic variability in the ‘Candidatus Pelagibacter ubique’ genome
    journal, May 2008

    • Gilbert, Jack A.; Mühling, Martin; Joint, Ian
    • The ISME Journal, Vol. 2, Issue 7
    • DOI: 10.1038/ismej.2008.49

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    journal, January 2010

    • Newton, Ryan J.; Griffin, Laura E.; Bowles, Kathy M.
    • The ISME Journal, Vol. 4, Issue 6
    • DOI: 10.1038/ismej.2009.150

    Dissimilatory reduction of nitrate in seawater by a Methylophaga strain containing two highly divergent narG sequences
    journal, April 2010

    • Auclair, Julie; Lépine, François; Parent, Serge
    • The ISME Journal, Vol. 4, Issue 10
    • DOI: 10.1038/ismej.2010.47

    Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease
    journal, April 2011

    • Wang, Zeneng; Klipfell, Elizabeth; Bennett, Brian J.
    • Nature, Vol. 472, Issue 7341
    • DOI: 10.1038/nature09922

    Novel pathway for assimilation of dimethylsulphoniopropionate widespread in marine bacteria
    journal, May 2011

    • Reisch, Chris R.; Stoudemayer, Melissa J.; Varaljay, Vanessa A.
    • Nature, Vol. 473, Issue 7346
    • DOI: 10.1038/nature10078

    Deltaproteobacteria (Pelobacter) and Methanococcoides are responsible for choline-dependent methanogenesis in a coastal saltmarsh sediment
    journal, September 2018


    Pyrrolysine in archaea: a 22nd amino acid encoded through a genetic code expansion
    journal, November 2018

    • Brugère, Jean-François; Atkins, John F.; O'Toole, Paul W.
    • Emerging Topics in Life Sciences, Vol. 2, Issue 4
    • DOI: 10.1042/etls20180094

    Organization of the genes involved in dimethylglycine and sarcosine degradation in Arthrobacter spp. : Implications for glycine betaine catabolism
    journal, June 2001


    Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme
    journal, November 2012

    • Craciun, S.; Balskus, E. P.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 52
    • DOI: 10.1073/pnas.1215689109

    Trimethylamine N-oxide metabolism by abundant marine heterotrophic bacteria
    journal, February 2014

    • Lidbury, I.; Murrell, J. C.; Chen, Y.
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 7
    • DOI: 10.1073/pnas.1317834111

    Coupled laboratory and field investigations resolve microbial interactions that underpin persistence in hydraulically fractured shales
    journal, June 2018

    • Borton, Mikayla A.; Hoyt, David W.; Roux, Simon
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 28
    • DOI: 10.1073/pnas.1800155115

    The rapid generation of mutation data matrices from protein sequences
    journal, January 1992


    Prognostic value of choline and betaine depends on intestinal microbiota-generated metabolite trimethylamine-N-oxide
    journal, February 2014


    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
    • DOI: 10.1093/gbe/evt128

    An Improved General Amino Acid Replacement Matrix
    journal, April 2008


    MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
    journal, October 2013

    • Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
    • Molecular Biology and Evolution, Vol. 30, Issue 12
    • DOI: 10.1093/molbev/mst197

    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
    • DOI: 10.1093/nar/gkh340

    Regulation of homocysteine metabolism and methylation in human and mouse tissues
    journal, August 2010

    • Chen, Natalie C.; Yang, Fan; Capecci, Louis M.
    • The FASEB Journal, Vol. 24, Issue 8
    • DOI: 10.1096/fj.09-143651

    Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti
    journal, January 1990


    A proteomic determination of cold adaptation in the Antarctic archaeon, Methanococcoides burtonii: Cold adaptation on an Antarctic archaeon
    journal, May 2004


    The BCCT family of carriers: from physiology to crystal structure: BCCT carriers
    journal, September 2010


    Bacterioplankton assemblages transforming dissolved organic compounds in coastal seawater
    journal, August 2007


    The Desulfitobacterium genus
    journal, September 2006


    Pyrrolysine Encoded by UAG in Archaea: Charging of a UAG-Decoding Specialized tRNA
    journal, May 2002


    Potential for Chemolithoautotrophy Among Ubiquitous Bacteria Lineages in the Dark Ocean
    journal, September 2011


    Osmotic control of glycine betaine biosynthesis and degradation in Rhizobium meliloti.
    journal, July 1988


    Isolation of two novel corrinoid proteins from acetate-grown Methanosarcina barkeri.
    journal, August 1993


    The Expanding World of Methylotrophic Metabolism
    journal, October 2009


    Carnitine--metabolism and functions
    journal, October 1983


    One Carbon Metabolism in SAR11 Pelagic Marine Bacteria
    journal, August 2011


    Archaebiotics: Proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease
    journal, October 2013

    • Brugère, Jean-François; Borrel, Guillaume; Gaci, Nadia
    • Gut Microbes, Vol. 5, Issue 1
    • DOI: 10.4161/gmic.26749

    Isolation and characterization of a tetramethylammonium-degrading Methanococcoides strain and a novel glycine betaine-utilizing Methanolobus strain
    journal, October 2014

    • Ticak, Tomislav; Hariraju, Dinesh; Arcelay, Margarette Bayron
    • Archives of Microbiology, Vol. 197, Issue 2
    • DOI: 10.1007/s00203-014-1043-6

    Deltaproteobacteria (Pelobacter) and Methanococcoides are responsible for choline-dependent methanogenesis in a coastal saltmarsh sediment
    journal, September 2018


    Pyrrolysine in archaea: a 22nd amino acid encoded through a genetic code expansion
    journal, November 2018

    • Brugère, Jean-François; Atkins, John F.; O'Toole, Paul W.
    • Emerging Topics in Life Sciences, Vol. 2, Issue 4
    • DOI: 10.1042/etls20180094

    A new family of uncultivated bacteria involved in methanogenesis from the ubiquitous osmolyte glycine betaine in coastal saltmarsh sediments
    journal, August 2019