Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans.
Journal
PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
04
09
2019
accepted:
04
02
2020
revised:
05
03
2020
pubmed:
25
2
2020
medline:
15
5
2020
entrez:
25
2
2020
Statut:
epublish
Résumé
The enzyme methyl-coenzyme M reductase (MCR) plays an important role in mediating global levels of methane by catalyzing a reversible reaction that leads to the production or consumption of this potent greenhouse gas in methanogenic and methanotrophic archaea. In methanogenic archaea, the alpha subunit of MCR (McrA) typically contains four to six posttranslationally modified amino acids near the active site. Recent studies have identified enzymes performing two of these modifications (thioglycine and 5-[S]-methylarginine), yet little is known about the formation and function of the remaining posttranslationally modified residues. Here, we provide in vivo evidence that a dedicated S-adenosylmethionine-dependent methyltransferase encoded by a gene we designated methylcysteine modification (mcmA) is responsible for formation of S-methylcysteine in Methanosarcina acetivorans McrA. Phenotypic analysis of mutants incapable of cysteine methylation suggests that the S-methylcysteine residue might play a role in adaption to mesophilic conditions. To examine the interactions between the S-methylcysteine residue and the previously characterized thioglycine, 5-(S)-methylarginine modifications, we generated M. acetivorans mutants lacking the three known modification genes in all possible combinations. Phenotypic analyses revealed complex, physiologically relevant interactions between the modified residues, which alter the thermal stability of MCR in a combinatorial fashion that is not readily predictable from the phenotypes of single mutants. High-resolution crystal structures of inactive MCR lacking the modified amino acids were indistinguishable from the fully modified enzyme, suggesting that interactions between the posttranslationally modified residues do not exert a major influence on the static structure of the enzyme but rather serve to fine-tune the activity and efficiency of MCR.
Identifiants
pubmed: 32092071
doi: 10.1371/journal.pbio.3000507
pii: PBIOLOGY-D-19-02599
pmc: PMC7058361
doi:
Substances chimiques
Amino Acids
0
Archaeal Proteins
0
Protein Subunits
0
Oxidoreductases
EC 1.-
Methyltransferases
EC 2.1.1.-
methyl coenzyme M reductase
EC 2.8.4.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
e3000507Subventions
Organisme : NIGMS NIH HHS
ID : R01 GM097142
Pays : United States
Organisme : NCRR NIH HHS
ID : S10 RR027109
Pays : United States
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
Proc Natl Acad Sci U S A. 2018 Mar 20;115(12):3030-3035
pubmed: 29507203
Appl Environ Microbiol. 1998 Feb;64(2):768-70
pubmed: 9464421
Science. 2016 May 20;352(6288):953-8
pubmed: 27199421
Angew Chem Int Ed Engl. 2016 Aug 26;55(36):10630-3
pubmed: 27467699
Ann N Y Acad Sci. 2008 Mar;1125:171-89
pubmed: 18378594
Annu Rev Microbiol. 2009;63:311-34
pubmed: 19575572
J Bacteriol. 2020 Jan 15;202(3):
pubmed: 31740491
Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2626-31
pubmed: 9122246
J Bacteriol. 2017 Jul 25;199(16):
pubmed: 28559298
J Biol Chem. 2019 Aug 2;294(31):11712-11725
pubmed: 31113866
Nat Rev Microbiol. 2019 Apr;17(4):219-232
pubmed: 30664670
Nat Microbiol. 2019 Apr;4(4):603-613
pubmed: 30833729
Elife. 2017 Sep 07;6:
pubmed: 28880150
Science. 1997 Nov 21;278(5342):1457-62
pubmed: 9367957
Front Microbiol. 2016 Apr 29;7:563
pubmed: 27199908
Nat Commun. 2019 Apr 23;10(1):1822
pubmed: 31015394
Nat Rev Microbiol. 2008 Aug;6(8):579-91
pubmed: 18587410
Science. 2016 Apr 1;352(6281):80-4
pubmed: 26966190
Nature. 2010 Jun 3;465(7298):606-8
pubmed: 20520712
J Biol Chem. 2000 Feb 11;275(6):3755-60
pubmed: 10660523
Methods Enzymol. 2018;613:325-347
pubmed: 30509472
J Biol Inorg Chem. 2005 Jun;10(4):333-42
pubmed: 15846525
Environ Microbiol. 2000 Oct;2(5):477-84
pubmed: 11233156
Nature. 2011 Nov 27;481(7379):98-101
pubmed: 22121022
Appl Environ Microbiol. 1993 Nov;59(11):3832-9
pubmed: 16349092
ISME J. 2019 May;13(5):1269-1279
pubmed: 30651609
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
J Mol Biol. 2000 Oct 20;303(2):329-44
pubmed: 11023796
Eur J Biochem. 1997 Jan 15;243(1-2):110-4
pubmed: 9030728
Curr Protoc Protein Sci. 2015 Feb 02;79:28.9.1-28.9.14
pubmed: 25640896
Sci Rep. 2018 May 9;8(1):7404
pubmed: 29743535
Nature. 2016 Nov 17;539(7629):396-401
pubmed: 27749816
Nature. 2019 Apr;568(7750):108-111
pubmed: 30918404
Nature. 2017 Mar 2;543(7643):78-82
pubmed: 28225763
J Mol Biol. 2001 May 25;309(1):315-30
pubmed: 11491299
Proc Natl Acad Sci U S A. 2017 Mar 14;114(11):2976-2981
pubmed: 28265068
Biochemistry. 1998 Feb 24;37(8):2639-47
pubmed: 9485414
FEBS J. 2007 Sep;274(18):4913-21
pubmed: 17725644
Science. 2016 Oct 21;354(6310):339-342
pubmed: 27846569
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147
Microb Biotechnol. 2017 Jan;10(1):9-10
pubmed: 27748569
J Am Chem Soc. 2016 Aug 3;138(30):9327-40
pubmed: 27366961
Biochemistry. 2019 Dec 31;58(52):5198-5220
pubmed: 30951290
Antimicrob Agents Chemother. 2012 Aug;56(8):4175-83
pubmed: 22615277