RNA-Dependent Cysteine Biosynthesis in Bacteria and Archaea.

Takahito Mukai,Takuya Umehara,Natalia N Ivanova,Dieter Söll,Ana Crnković,Nikos C Kyrpides

doi:10.1128/mbio.00561-17

Takahito Mukai, Takuya Umehara + Show 4 more

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https://doi.org/10.1128/mbio.00561-17

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Abstract

ABSTRACTThe diversity of the genetic code systems used by microbes on earth is yet to be elucidated. It is known that certain methanogenic archaea employ an alternative system for cysteine (Cys) biosynthesis and encoding; tRNACys is first acylated with phosphoserine (Sep) by O-phosphoseryl-tRNA synthetase (SepRS) and then converted to Cys-tRNACys by Sep-tRNA:Cys-tRNA synthase (SepCysS). In this study, we searched all genomic and metagenomic protein sequence data in the Integrated Microbial Genomes (IMG) system and at the NCBI to reveal new clades of SepRS and SepCysS proteins belonging to diverse archaea in the four major groups (DPANN, Euryarchaeota, TACK, and Asgard) and two groups of bacteria (“Candidatus Parcubacteria” and Chloroflexi). Bacterial SepRS and SepCysS charged bacterial tRNACys species with cysteine in vitro. Homologs of SepCysE, a scaffold protein facilitating SepRS⋅SepCysS complex assembly in Euryarchaeota class I methanogens, are found in a few groups of TACK and Asgard archaea, whereas the C-terminally truncated homologs exist fused or genetically coupled with diverse SepCysS species. Investigation of the selenocysteine (Sec)- and pyrrolysine (Pyl)-utilizing traits in SepRS-utilizing archaea and bacteria revealed that the archaea carrying full-length SepCysE employ Sec and that SepRS is often found in Pyl-utilizing archaea and Chloroflexi bacteria. We discuss possible contributions of the SepRS-SepCysS system for sulfur assimilation, methanogenesis, and other metabolic processes requiring large amounts of iron-sulfur enzymes or Pyl-containing enzymes.

Highlights

The diversity of the genetic code systems used by microbes on earth is yet to be elucidated
A SepRS-Sep-tRNA:Cys-tRNA synthase (SepCysS) operon was found in a metagenomic bin of a candidate phylum radiation (CPR) bacterium, “Candidatus Parcubacteria” bacterium DG_74_2 [39]
This “Ca. Parcubacteria” DG_74_2 bin is apparently composed of a few different genomes, including those of two “Ca. Parcubacteria” species, the SepRS-SepCysS operon is flanked by a typical “Ca. Parcubacteria” gene encoding a signal transduction histidine kinase

Summary

Introduction

The diversity of the genetic code systems used by microbes on earth is yet to be elucidated. Homologs of SepCysE, a scaffold protein facilitating SepRS·SepCysS complex assembly in Euryarchaeota class I methanogens, are found in a few groups of TACK and Asgard archaea, whereas the C-terminally truncated homologs exist fused or genetically coupled with diverse SepCysS species. IMPORTANCE Comprehensive analyses of all genomic and metagenomic protein sequence data in public databases revealed the distribution and evolution of an alternative cysteine-encoding system in diverse archaea and bacteria. Our results provide additional bioinformatic evidence for the contribution of the SepRS-SepCysS system for sulfur assimilation and diverse metabolisms which require vast amounts of iron-sulfur enzymes and proteins. Among these biological activities, methanogenesis, methylamine metabolism, and organohalide respiration may have local and global effects on earth. Phylogenetic studies of organisms based on protein sequences challenge traditional phylogenies based solely on rRNA sequences [29]

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