Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria

Mukai, Takahito; Reynolds, Noah; Crnković, Ana; Söll, Dieter

doi:10.3390/life7010008

Title: Bioinformatic Analysis Reveals Archaeal tRNA^Tyr and tRNA^Trp Identities in Bacteria

Abstract

The tRNA identity elements for some amino acids are distinct between the bacterial and archaeal domains. Searching in recent genomic and metagenomic sequence data, we found some candidate phyla radiation (CPR) bacteria with archaeal tRNA identity for Tyr-tRNA and Trp-tRNA synthesis. These bacteria possess genes for tyrosyl-tRNA synthetase (TyrRS) and tryptophanyl-tRNA synthetase (TrpRS) predicted to be derived from DPANN superphylum archaea, while the cognate tRNA^Tyr and tRNA^Trp genes reveal bacterial or archaeal origins. We identified a trace of domain fusion and swapping in the archaeal-type TyrRS gene of a bacterial lineage, suggesting that CPR bacteria may have used this mechanism to create diverse proteins. Archaeal-type TrpRS of bacteria and a few TrpRS species of DPANN archaea represent a new phylogenetic clade (named TrpRS-A). The TrpRS-A open reading frames (ORFs) are always associated with another ORF (named ORF1) encoding an unknown protein without global sequence identity to any known protein. However, our protein structure prediction identified a putative HIGH-motif and KMSKS-motif as well as many α-helices that are characteristic of class I aminoacyl-tRNA synthetase (aaRS) homologs. These results provide another example of the diversity of molecular components that implement the genetic code and provide a clue to the early evolution ofmore » life and the genetic code.« less

Authors:

Mukai, Takahito ^[1]; Reynolds, Noah ^[1]; Crnković, Ana ^[1]; Söll, Dieter ^[2]

Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry
Yale Univ., New Haven, CT (United States). Dept. of Molecular Biophysics and Biochemistry and Dept. of Chemistry

Publication Date:: Tue Feb 21 00:00:00 EST 2017

Research Org.:: Yale Univ., New Haven, CT (United States)

Sponsoring Org.:: National Institute of General Medical Sciences (NIGMS); USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; Japan Society for the Promotion of Science (JSPS)

OSTI Identifier:: 1628396

Grant/Contract Number:: FG02-98ER20311; GM22854

Resource Type:: Accepted Manuscript

Journal Name:: Life

Additional Journal Information:: Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 2075-1729

Publisher:: MDPI

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Life sciences & biomedicine - other topics; Microbiology; tRNA; aaRS; genetic code; evolution; lateral gene transfer

Citation Formats


                    Mukai, Takahito, Reynolds, Noah, Crnković, Ana, and Söll, Dieter. Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria.  United States: N. p., 2017. 
Web.  doi:10.3390/life7010008.

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                    Mukai, Takahito, Reynolds, Noah, Crnković, Ana, & Söll, Dieter. Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria.  United States.  https://doi.org/10.3390/life7010008

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                    Mukai, Takahito, Reynolds, Noah, Crnković, Ana, and Söll, Dieter. Tue .  
"Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria".  United States.  https://doi.org/10.3390/life7010008.  https://www.osti.gov/servlets/purl/1628396.

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@article{osti_1628396,

  title        = {Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria},

  author       = {Mukai, Takahito and Reynolds, Noah and Crnković, Ana and Söll, Dieter},

  abstractNote = {The tRNA identity elements for some amino acids are distinct between the bacterial and archaeal domains. Searching in recent genomic and metagenomic sequence data, we found some candidate phyla radiation (CPR) bacteria with archaeal tRNA identity for Tyr-tRNA and Trp-tRNA synthesis. These bacteria possess genes for tyrosyl-tRNA synthetase (TyrRS) and tryptophanyl-tRNA synthetase (TrpRS) predicted to be derived from DPANN superphylum archaea, while the cognate tRNATyr and tRNATrp genes reveal bacterial or archaeal origins. We identified a trace of domain fusion and swapping in the archaeal-type TyrRS gene of a bacterial lineage, suggesting that CPR bacteria may have used this mechanism to create diverse proteins. Archaeal-type TrpRS of bacteria and a few TrpRS species of DPANN archaea represent a new phylogenetic clade (named TrpRS-A). The TrpRS-A open reading frames (ORFs) are always associated with another ORF (named ORF1) encoding an unknown protein without global sequence identity to any known protein. However, our protein structure prediction identified a putative HIGH-motif and KMSKS-motif as well as many α-helices that are characteristic of class I aminoacyl-tRNA synthetase (aaRS) homologs. These results provide another example of the diversity of molecular components that implement the genetic code and provide a clue to the early evolution of life and the genetic code.},

  doi          = {10.3390/life7010008},

  journal      = {Life},

  number       = 1,

  volume       = 7,

  place        = {United States},

  year         = {Tue Feb 21 00:00:00 EST 2017},

  month        = {Tue Feb 21 00:00:00 EST 2017}

}

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Title: Bioinformatic Analysis Reveals Archaeal tRNATyr and tRNATrp Identities in Bacteria

Abstract

Citation Formats

Universal rules and idiosyncratic features in tRNA identity journal, November 1998

Residues Lys-149 and Glu-153 Switch the Aminoacylation of tRNATrp in Bacillus subtilis journal, July 2004

An unusual tryptophanyl tRNA synthetase interacts with nitric oxide synthase in Deinococcus radiodurans journal, November 2004

IMG/M 4 version of the integrated metagenome comparative analysis system journal, October 2013

An SHR–SCR module specifies legume cortical cell fate to enable nodulation journal, December 2020

Biased gene transfer in microbial evolution journal, June 2011

Clustal W and Clustal X version 2.0 journal, September 2007

Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion journal, May 2003

A role for [Fe4S4] clusters in tRNA recognition—a theoretical study text, January 2014

OB or Not OB: Idiosyncratic utilization of the tRNA-binding OB-fold domain in unicellular, pathogenic eukaryotes journal, October 2016

Functional replacement of the endogenous tyrosyl-tRNA synthetase–tRNATyr pair by the archaeal tyrosine pair in Escherichia coli for genetic code expansion journal, February 2010

The complex evolutionary history of aminoacyl-tRNA synthetases journal, November 2016

Aminoacyl-tRNA-Utilizing Enzymes in Natural Product Biosynthesis journal, January 2017

Human mitochondrial TyrRS disobeys the tyrosine identity rules journal, May 2005

Species-specific differences in the operational RNA code for aminoacylation of tRNATrp journal, October 2001

SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information text, January 2014

Η πολύπλοκη εξελικτική πορεία των συνθετασών του αμινοάκυλο-tRNA other, January 2017

Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process journal, March 2000

JPred4: a protein secondary structure prediction server journal, April 2015

An orthogonalized platform for genetic code expansion in both bacteria and eukaryotes journal, February 2017

Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion [遺伝暗号拡張に関わるチロシルtRNA合成酵素の直交性の構造的基盤] journal, January 2003

Structure and activity of an aminoacyl-tRNA synthetase that charges tRNA with nitro-tryptophan journal, February 2005

Virus-Encoded Aminoacyl-tRNA Synthetases: Structural and Functional Characterization of Mimivirus TyrRS and MetRS journal, September 2007

SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building journal, October 2009

Maintaining genetic code through adaptations of tRNA synthetases to taxonomic domains journal, December 1997

Change of tRNA identity leads to a divergent orthogonal histidyl-tRNA synthetase/tRNAHis pair journal, November 2010

Comparison of super-secondary structures in proteins journal, May 1973

Cpf1 Is a Single RNA-Guided Endonuclease of a Class 2 CRISPR-Cas System journal, October 2015

Evidence that two present-day components needed for the genetic code appeared after nucleated cells separated from eubacteria. journal, January 1996

Ancestral Reconstruction of a Pre-LUCA Aminoacyl-tRNA Synthetase Ancestor Supports the Late Addition of Trp to the Genetic Code journal, March 2015

Unusual biology across a group comprising more than 15% of domain Bacteria journal, June 2015

Trans-oligomerization of duplicated aminoacyl-tRNA synthetases maintains genetic code fidelity under stress journal, October 2015

Metagenomics uncovers gaps in amplicon-based detection of microbial diversity journal, February 2016

Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life journal, October 2014

Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases journal, November 2016

A new view of the tree of life journal, April 2016

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets journal, March 2016

The Double-Length Tyrosyl-tRNA Synthetase from the Eukaryote Leishmania major Forms an Intrinsically Asymmetric Pseudo-Dimer journal, June 2011

Crystal Structure of Human Mitochondrial Tyrosyl-tRNA Synthetase Reveals Common and Idiosyncratic Features journal, November 2007

Loss of a Universal tRNA Feature journal, December 2006

Indolmycin Resistance of Streptomyces coelicolor A3(2) by Induced Expression of One of Its Two Tryptophanyl-tRNA Synthetases journal, April 2002

TFAM detects co-evolution of tRNA identity rules with lateral transfer of histidyl-tRNA synthetase journal, February 2006

SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information journal, April 2014

A Eubacterial Mycobacterium tuberculosis tRNA Synthetase Is Eukaryote-like and Resistant to a Eubacterial-Specific Antisynthetase Drug † journal, January 1996

Phenylalanyl-tRNA Synthetase Contains a Dispensable RNA-Binding Domain that Contributes to the Editing of Noncognate Aminoacyl-tRNA † journal, August 2006

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal, October 2016

A role for [Fe4S4] clusters in tRNA recognition—a theoretical study journal, April 2014

Complete Genome Sequence of Clostridium botulinum CJ0611A1, a Type A(B) Isolate Associated with an International Outbreak of Botulism from Commercial Carrot Juice journal, January 2021

Structure of a tryptophanyl-tRNA synthetase containing an iron–sulfur cluster journal, September 2010

Bipartite graph analyses reveal interdomain LGT involving ultrasmall prokaryotes and their divergent, membrane-related proteins: LGT among ultrasmall prokaryotes journal, August 2016

RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria journal, May 2016

Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains journal, December 2003

Evolution of the tRNATyr/TyrRS aminoacylation systems journal, September 2005

Identity elements of tRNA(Trp). Identification and evolutionary conservation journal, May 1993

Evolution of Aminoacyl-tRNA Synthetases—Analysis of Unique Domain Architectures and Phylogenetic Trees Reveals a Complex History of Horizontal Gene Transfer Events journal, August 1999

Information theory unveils the evolution of tRNA identity elements in the three domains of life journal, September 2019

Identity Elements of tRNA as Derived from Information Analysis journal, June 2017

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations journal, September 2018

Title: Bioinformatic Analysis Reveals Archaeal tRNA^Tyr and tRNA^Trp Identities in Bacteria

Universal rules and idiosyncratic features in tRNA identity
journal, November 1998

Residues Lys-149 and Glu-153 Switch the Aminoacylation of tRNATrp in Bacillus subtilis
journal, July 2004

An unusual tryptophanyl tRNA synthetase interacts with nitric oxide synthase in Deinococcus radiodurans
journal, November 2004

IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013

An SHR–SCR module specifies legume cortical cell fate to enable nodulation
journal, December 2020

Biased gene transfer in microbial evolution
journal, June 2011

Clustal W and Clustal X version 2.0
journal, September 2007

Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion
journal, May 2003

A role for [Fe4S4] clusters in tRNA recognition—a theoretical study
text, January 2014

OB or Not OB: Idiosyncratic utilization of the tRNA-binding OB-fold domain in unicellular, pathogenic eukaryotes
journal, October 2016

Functional replacement of the endogenous tyrosyl-tRNA synthetase–tRNATyr pair by the archaeal tyrosine pair in Escherichia coli for genetic code expansion
journal, February 2010

The complex evolutionary history of aminoacyl-tRNA synthetases
journal, November 2016

Aminoacyl-tRNA-Utilizing Enzymes in Natural Product Biosynthesis
journal, January 2017

Human mitochondrial TyrRS disobeys the tyrosine identity rules
journal, May 2005

Species-specific differences in the operational RNA code for aminoacylation of tRNATrp
journal, October 2001

SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information
text, January 2014

Η πολύπλοκη εξελικτική πορεία των συνθετασών του αμινοάκυλο-tRNA
other, January 2017

Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process
journal, March 2000

JPred4: a protein secondary structure prediction server
journal, April 2015

An orthogonalized platform for genetic code expansion in both bacteria and eukaryotes
journal, February 2017

Structural basis for orthogonal tRNA specificities of tyrosyl-tRNA synthetases for genetic code expansion [遺伝暗号拡張に関わるチロシルtRNA合成酵素の直交性の構造的基盤]
journal, January 2003

Structure and activity of an aminoacyl-tRNA synthetase that charges tRNA with nitro-tryptophan
journal, February 2005

Virus-Encoded Aminoacyl-tRNA Synthetases: Structural and Functional Characterization of Mimivirus TyrRS and MetRS
journal, September 2007

SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building
journal, October 2009

Maintaining genetic code through adaptations of tRNA synthetases to taxonomic domains
journal, December 1997

Change of tRNA identity leads to a divergent orthogonal histidyl-tRNA synthetase/tRNAHis pair
journal, November 2010

Comparison of super-secondary structures in proteins
journal, May 1973

Cpf1 Is a Single RNA-Guided Endonuclease of a Class 2 CRISPR-Cas System
journal, October 2015

Evidence that two present-day components needed for the genetic code appeared after nucleated cells separated from eubacteria.
journal, January 1996

Ancestral Reconstruction of a Pre-LUCA Aminoacyl-tRNA Synthetase Ancestor Supports the Late Addition of Trp to the Genetic Code
journal, March 2015

Unusual biology across a group comprising more than 15% of domain Bacteria
journal, June 2015

Trans-oligomerization of duplicated aminoacyl-tRNA synthetases maintains genetic code fidelity under stress
journal, October 2015

Metagenomics uncovers gaps in amplicon-based detection of microbial diversity
journal, February 2016

Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life
journal, October 2014

Quest for Ancestors of Eukaryal Cells Based on Phylogenetic Analyses of Aminoacyl-tRNA Synthetases
journal, November 2016

A new view of the tree of life
journal, April 2016

MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016

The Double-Length Tyrosyl-tRNA Synthetase from the Eukaryote Leishmania major Forms an Intrinsically Asymmetric Pseudo-Dimer
journal, June 2011

Crystal Structure of Human Mitochondrial Tyrosyl-tRNA Synthetase Reveals Common and Idiosyncratic Features
journal, November 2007

Loss of a Universal tRNA Feature
journal, December 2006

Indolmycin Resistance of Streptomyces coelicolor A3(2) by Induced Expression of One of Its Two Tryptophanyl-tRNA Synthetases
journal, April 2002

TFAM detects co-evolution of tRNA identity rules with lateral transfer of histidyl-tRNA synthetase
journal, February 2006

SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information
journal, April 2014

A Eubacterial Mycobacterium tuberculosis tRNA Synthetase Is Eukaryote-like and Resistant to a Eubacterial-Specific Antisynthetase Drug ^†
journal, January 1996

Phenylalanyl-tRNA Synthetase Contains a Dispensable RNA-Binding Domain that Contributes to the Editing of Noncognate Aminoacyl-tRNA ^†
journal, August 2006

Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system
journal, October 2016

A role for [Fe4S4] clusters in tRNA recognition—a theoretical study
journal, April 2014

Complete Genome Sequence of Clostridium botulinum CJ0611A1, a Type A(B) Isolate Associated with an International Outbreak of Botulism from Commercial Carrot Juice
journal, January 2021

Structure of a tryptophanyl-tRNA synthetase containing an iron–sulfur cluster
journal, September 2010

Bipartite graph analyses reveal interdomain LGT involving ultrasmall prokaryotes and their divergent, membrane-related proteins: LGT among ultrasmall prokaryotes
journal, August 2016

RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria
journal, May 2016

Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains
journal, December 2003

Evolution of the tRNATyr/TyrRS aminoacylation systems
journal, September 2005

Identity elements of tRNA(Trp). Identification and evolutionary conservation
journal, May 1993

Evolution of Aminoacyl-tRNA Synthetases—Analysis of Unique Domain Architectures and Phylogenetic Trees Reveals a Complex History of Horizontal Gene Transfer Events
journal, August 1999

Information theory unveils the evolution of tRNA identity elements in the three domains of life
journal, September 2019

Identity Elements of tRNA as Derived from Information Analysis
journal, June 2017

Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations
journal, September 2018