Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans

Nayak, Dipti D.; Liu, Andi; Agrawal, Neha; Rodriguez-Carerro, Roy; Dong, Shi-Hui; Mitchell, Douglas A.; Nair, Satish K.; Metcalf, William W.; Sass, ed., Henrik

doi:10.1371/journal.pbio.3000507

Title: Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans

Journal Article · Mon Feb 24 00:00:00 EST 2020 · PLoS Biology (Online)

DOI:https://doi.org/10.1371/journal.pbio.3000507· OSTI ID:1603218

Nayak, Dipti D.;

;

; Dong, Shi-Hui;

; Nair, Satish K.;

; Sass, ed., Henrik

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.

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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)

Grant/Contract Number:: FG02-02ER15296

OSTI ID:: 1603218

Alternate ID(s):: OSTI ID: 1601490; OSTI ID: 1800037

Journal Information:: PLoS Biology (Online), Journal Name: PLoS Biology (Online) Vol. 18 Journal Issue: 2; ISSN 1545-7885

Publisher:: Public Library of Science (PLoS)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 23 works

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Title: Functional interactions between posttranslationally modified amino acids of methyl-coenzyme M reductase in Methanosarcina acetivorans

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