Identification of the 3-amino-3-carboxypropyl (acp) transferase enzyme responsible for acp3U formation at position 47 in Escherichia coli tRNAs

Abstract

AbstracttRNAs from all domains of life contain modified nucleotides. However, even for the experimentally most thoroughly characterized model organism Escherichia coli not all tRNA modification enzymes are known. In particular, no enzyme has been found yet for introducing the acp3U modification at position 47 in the variable loop of eight E. coli tRNAs. Here we identify the so far functionally uncharacterized YfiP protein as the SAM-dependent 3-amino-3-carboxypropyl transferase catalyzing this modification and thereby extend the list of known tRNA modification enzymes in E. coli. Similar to the Tsr3 enzymes that introduce acp modifications at U or m1Ψ nucleotides in rRNAs this protein contains a DTW domain suggesting that acp transfer reactions to RNA nucleotides are a general function of DTW domain containing proteins. The introduction of the acp3U-47 modification in E. coli tRNAs is promoted by the presence of the m7G-46 modification as well as by growth in rich medium. However, a deletion of the enzymes responsible for the modifications at position 46 and 47 in the variable loop of E. coli tRNAs did not lead to a clearly discernible phenotype suggesting that these two modifications play only a minor role in ensuring the proper function of tRNAs in E. coli.

Autoren

Britta Meyer
Carina Immer
Steffen Kaiser
Sunny Sharma
Jun Yang
Peter Watzinger
Lena Weiß
Annika Kotter
Mark Helm
Hans-Michael Seitz
Peter Kötter
Stefanie Kellner
Karl-Dieter Entian
Jens Wöhnert

DOI

10.1093/nar/gkz1191

eISSN

1362-4962

ISSN

0305-1048

Ausgabe der Veröffentlichung

3

Zeitschrift

Nucleic Acids Research

Sprache

en

Online publication date

2019

Paginierung

1435 - 1450

Datum der Veröffentlichung

2020

Status

Published

Herausgeber

Oxford University Press (OUP)

Herausgeber URL

http://dx.doi.org/10.1093/nar/gkz1191

Datum der Datenerfassung

2023

Titel

Identification of the 3-amino-3-carboxypropyl (acp) transferase enzyme responsible for acp3U formation at position 47 in Escherichia coli tRNAs

Ausgabe der Zeitschrift

48

Datenquelle: Crossref

Abstract

tRNAs from all domains of life contain modified nucleotides. However, even for the experimentally most thoroughly characterized model organism Escherichia coli not all tRNA modification enzymes are known. In particular, no enzyme has been found yet for introducing the acp3U modification at position 47 in the variable loop of eight E. coli tRNAs. Here we identify the so far functionally uncharacterized YfiP protein as the SAM-dependent 3-amino-3-carboxypropyl transferase catalyzing this modification and thereby extend the list of known tRNA modification enzymes in E. coli. Similar to the Tsr3 enzymes that introduce acp modifications at U or m1Ψ nucleotides in rRNAs this protein contains a DTW domain suggesting that acp transfer reactions to RNA nucleotides are a general function of DTW domain containing proteins. The introduction of the acp3U-47 modification in E. coli tRNAs is promoted by the presence of the m7G-46 modification as well as by growth in rich medium. However, a deletion of the enzymes responsible for the modifications at position 46 and 47 in the variable loop of E. coli tRNAs did not lead to a clearly discernible phenotype suggesting that these two modifications play only a minor role in ensuring the proper function of tRNAs in E. coli.

Addresses

Institute for Molecular Biosciences, Goethe-Universität Frankfurt, Max-von-Laue-Str. 9, 60438 Frankfurt/M., Germany.

Autoren

Britta Meyer
Carina Immer
Steffen Kaiser
Sunny Sharma
Jun Yang
Peter Watzinger
Lena Weiß
Annika Kotter
Mark Helm
Hans-Michael Seitz
Peter Kötter
Stefanie Kellner
Karl-Dieter Entian
Jens Wöhnert

DOI

10.1093/nar/gkz1191

eISSN

1362-4962

Externe Identifier

PubMed Identifier: 31863583
PubMed Central ID: PMC7026641

Funding acknowledgements

Deutsche Forschungsgemeinschaft: Wo901/7-1
Deutsche Forschungsgemeinschaft: Ke1943/4-1
Deutsche Forschungsgemeinschaft: Ke1943/3-1
Deutsche Forschungsgemeinschaft: En134/16-1

Open access

true

ISSN

0305-1048

Ausgabe der Veröffentlichung

3

Zeitschrift

Nucleic acids research

Schlüsselwörter

Escherichia coli
Saccharomyces cerevisiae
Alkyl and Aryl Transferases
Nucleotides
Bacterial Proteins
RNA, Transfer
Nucleic Acid Conformation

Sprache

eng

Medium

Print

Open access status

Open Access

Paginierung

1435 - 1450

Datum der Veröffentlichung

2020

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2019

Titel

Identification of the 3-amino-3-carboxypropyl (acp) transferase enzyme responsible for acp3U formation at position 47 in Escherichia coli tRNAs.

Sub types

Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

48

Files

https://academic.oup.com/nar/article-pdf/48/3/1435/32504979/gkz1191.pdf https://europepmc.org/articles/PMC7026641?pdf=render

Datenquelle: Europe PubMed Central

Abstract

tRNAs from all domains of life contain modified nucleotides. However, even for the experimentally most thoroughly characterized model organism Escherichia coli not all tRNA modification enzymes are known. In particular, no enzyme has been found yet for introducing the acp3U modification at position 47 in the variable loop of eight E. coli tRNAs. Here we identify the so far functionally uncharacterized YfiP protein as the SAM-dependent 3-amino-3-carboxypropyl transferase catalyzing this modification and thereby extend the list of known tRNA modification enzymes in E. coli. Similar to the Tsr3 enzymes that introduce acp modifications at U or m1Ψ nucleotides in rRNAs this protein contains a DTW domain suggesting that acp transfer reactions to RNA nucleotides are a general function of DTW domain containing proteins. The introduction of the acp3U-47 modification in E. coli tRNAs is promoted by the presence of the m7G-46 modification as well as by growth in rich medium. However, a deletion of the enzymes responsible for the modifications at position 46 and 47 in the variable loop of E. coli tRNAs did not lead to a clearly discernible phenotype suggesting that these two modifications play only a minor role in ensuring the proper function of tRNAs in E. coli.

Date of acceptance

2019

Autoren

Britta Meyer
Carina Immer
Steffen Kaiser
Sunny Sharma
Jun Yang
Peter Watzinger
Lena Weiß
Annika Kotter
Mark Helm
Hans-Michael Seitz
Peter Kötter
Stefanie Kellner
Karl-Dieter Entian
Jens Wöhnert

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/31863583

DOI

10.1093/nar/gkz1191

eISSN

1362-4962

Externe Identifier

PubMed Central ID: PMC7026641

Ausgabe der Veröffentlichung

3

Zeitschrift

Nucleic Acids Res

Schlüsselwörter

Alkyl and Aryl Transferases
Bacterial Proteins
Escherichia coli
Nucleic Acid Conformation
Nucleotides
RNA, Transfer
Saccharomyces cerevisiae

Sprache

eng

Country

England

Paginierung

1435 - 1450

PII

5682905

Datum der Veröffentlichung

2020

Status

Published

Datum, an dem der Datensatz öffentlich gemacht wurde

2020

Titel

Identification of the 3-amino-3-carboxypropyl (acp) transferase enzyme responsible for acp3U formation at position 47 in Escherichia coli tRNAs.

Sub types

Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

48

Datenquelle: PubMed

Identification of the 3-amino-3-carboxypropyl (acp) transferase enzyme responsible for acp3U formation at position 47 in Escherichia coli tRNAs

Files

Werkzeuge