The transcriptomic landscape of cupriavidus metallidurans CH34 acutely exposed to copper

Laurens Maertens; Natalie Leys; Jean Yves Matroule; Rob Van Houdt

doi:10.3390/genes11091049

The transcriptomic landscape of cupriavidus metallidurans CH34 acutely exposed to copper

Laurens Maertens
, Natalie Leys
, Jean Yves Matroule
, Rob Van Houdt

Research output: Contribution to journal › Article › peer-review

Abstract

Bacteria are increasingly used for biotechnological applications such as bioremediation, biorecovery, bioproduction, and biosensing. The development of strains suited for such applications requires a thorough understanding of their behavior, with a key role for their transcriptomic landscape. We present a thorough analysis of the transcriptome of Cupriavidus metallidurans CH34 cells acutely exposed to copper by tagRNA‐sequencing. C. metallidurans CH34 is a model organism for metal resistance, and its potential as a biosensor and candidate for metal bioremediation has been demonstrated in multiple studies. Several metabolic pathways were impacted by Cu exposure, and a broad spectrum of metal resistance mechanisms, not limited to copper‐specific clusters, was overexpressed. In addition, several gene clusters involved in the oxidative stress response and the cysteine‐sulfur metabolism were induced. In total, 7500 transcription start sites (TSSs) were annotated and classified with respect to their location relative to coding sequences (CDSs). Predicted TSSs were used to re‐annotate 182 CDSs. The TSSs of 2422 CDSs were detected, and consensus promotor logos were derived. Interestingly, many leaderless messenger RNAs (mRNAs) were found. In addition, many mRNAs were transcribed from multiple alternative TSSs. We observed pervasive intragenic TSSs both in sense and antisense to CDSs. Antisense transcripts were enriched near the 5′ end of mRNAs, indicating a functional role in post‐transcriptional regulation. In total, 578 TSSs were detected in intergenic regions, of which 35 were identified as putative small regulatory RNAs. Finally, we provide a detailed analysis of the main copper resistance clusters in CH34, which include many intragenic and antisense transcripts. These results clearly highlight the ubiquity of noncoding transcripts in the CH34 transcriptome, many of which are putatively involved in the regulation of metal resistance.

Original language	English
Article number	1049
Pages (from-to)	1-24
Number of pages	24
Journal	Genes
Volume	11
Issue number	9
DOIs	https://doi.org/10.3390/genes11091049
Publication status	Published - 4 Sept 2020

Funding

Funding: This research was supported by the European Space Agency (ESA‐PRODEX) and the Belgian Science Policy (Belspo) through the BIOFILMS project (C4000129318). LM was funded by a Fonds Spécial de la Recherche of UNamur. This research was supported by the European Space Agency (ESA?PRODEX) and the Belgian Science Policy (Belspo) through the BIOFILMS project (C4000129318). LM was funded by a Fonds Sp?cial de la Recherche of UNamur. Acknowledgments: We would like to thank J?rgen Claesen for fruitful advice regarding the data analysis of differential gene expression and transcription start sites.

Keywords

Copper
Cupriavidus metallidurans
Differential gene expression
Differential RNA‐sequencing
Gene regulation
SRNA
Transcription start site

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10.3390/genes11091049

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@article{c372b03734904ba7b7d248287aa7aa85,

title = "The transcriptomic landscape of cupriavidus metallidurans CH34 acutely exposed to copper",

abstract = "Bacteria are increasingly used for biotechnological applications such as bioremediation, biorecovery, bioproduction, and biosensing. The development of strains suited for such applications requires a thorough understanding of their behavior, with a key role for their transcriptomic landscape. We present a thorough analysis of the transcriptome of Cupriavidus metallidurans CH34 cells acutely exposed to copper by tagRNA‐sequencing. C. metallidurans CH34 is a model organism for metal resistance, and its potential as a biosensor and candidate for metal bioremediation has been demonstrated in multiple studies. Several metabolic pathways were impacted by Cu exposure, and a broad spectrum of metal resistance mechanisms, not limited to copper‐specific clusters, was overexpressed. In addition, several gene clusters involved in the oxidative stress response and the cysteine‐sulfur metabolism were induced. In total, 7500 transcription start sites (TSSs) were annotated and classified with respect to their location relative to coding sequences (CDSs). Predicted TSSs were used to re‐annotate 182 CDSs. The TSSs of 2422 CDSs were detected, and consensus promotor logos were derived. Interestingly, many leaderless messenger RNAs (mRNAs) were found. In addition, many mRNAs were transcribed from multiple alternative TSSs. We observed pervasive intragenic TSSs both in sense and antisense to CDSs. Antisense transcripts were enriched near the 5′ end of mRNAs, indicating a functional role in post‐transcriptional regulation. In total, 578 TSSs were detected in intergenic regions, of which 35 were identified as putative small regulatory RNAs. Finally, we provide a detailed analysis of the main copper resistance clusters in CH34, which include many intragenic and antisense transcripts. These results clearly highlight the ubiquity of noncoding transcripts in the CH34 transcriptome, many of which are putatively involved in the regulation of metal resistance.",

keywords = "Copper, Cupriavidus metallidurans, Differential gene expression, Differential RNA‐sequencing, Gene regulation, SRNA, Transcription start site",

author = "Laurens Maertens and Natalie Leys and Matroule, \{Jean Yves\} and \{Van Houdt\}, Rob",

note = "Publisher Copyright: {\textcopyright} 2020 by the authors. Licensee MDPI, Basel, Switzerland.",

year = "2020",

month = sep,

day = "4",

doi = "10.3390/genes11091049",

language = "English",

volume = "11",

pages = "1--24",

journal = "Genes",

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TY - JOUR

T1 - The transcriptomic landscape of cupriavidus metallidurans CH34 acutely exposed to copper

AU - Maertens, Laurens

AU - Leys, Natalie

AU - Matroule, Jean Yves

AU - Van Houdt, Rob

PY - 2020/9/4

Y1 - 2020/9/4

N2 - Bacteria are increasingly used for biotechnological applications such as bioremediation, biorecovery, bioproduction, and biosensing. The development of strains suited for such applications requires a thorough understanding of their behavior, with a key role for their transcriptomic landscape. We present a thorough analysis of the transcriptome of Cupriavidus metallidurans CH34 cells acutely exposed to copper by tagRNA‐sequencing. C. metallidurans CH34 is a model organism for metal resistance, and its potential as a biosensor and candidate for metal bioremediation has been demonstrated in multiple studies. Several metabolic pathways were impacted by Cu exposure, and a broad spectrum of metal resistance mechanisms, not limited to copper‐specific clusters, was overexpressed. In addition, several gene clusters involved in the oxidative stress response and the cysteine‐sulfur metabolism were induced. In total, 7500 transcription start sites (TSSs) were annotated and classified with respect to their location relative to coding sequences (CDSs). Predicted TSSs were used to re‐annotate 182 CDSs. The TSSs of 2422 CDSs were detected, and consensus promotor logos were derived. Interestingly, many leaderless messenger RNAs (mRNAs) were found. In addition, many mRNAs were transcribed from multiple alternative TSSs. We observed pervasive intragenic TSSs both in sense and antisense to CDSs. Antisense transcripts were enriched near the 5′ end of mRNAs, indicating a functional role in post‐transcriptional regulation. In total, 578 TSSs were detected in intergenic regions, of which 35 were identified as putative small regulatory RNAs. Finally, we provide a detailed analysis of the main copper resistance clusters in CH34, which include many intragenic and antisense transcripts. These results clearly highlight the ubiquity of noncoding transcripts in the CH34 transcriptome, many of which are putatively involved in the regulation of metal resistance.

AB - Bacteria are increasingly used for biotechnological applications such as bioremediation, biorecovery, bioproduction, and biosensing. The development of strains suited for such applications requires a thorough understanding of their behavior, with a key role for their transcriptomic landscape. We present a thorough analysis of the transcriptome of Cupriavidus metallidurans CH34 cells acutely exposed to copper by tagRNA‐sequencing. C. metallidurans CH34 is a model organism for metal resistance, and its potential as a biosensor and candidate for metal bioremediation has been demonstrated in multiple studies. Several metabolic pathways were impacted by Cu exposure, and a broad spectrum of metal resistance mechanisms, not limited to copper‐specific clusters, was overexpressed. In addition, several gene clusters involved in the oxidative stress response and the cysteine‐sulfur metabolism were induced. In total, 7500 transcription start sites (TSSs) were annotated and classified with respect to their location relative to coding sequences (CDSs). Predicted TSSs were used to re‐annotate 182 CDSs. The TSSs of 2422 CDSs were detected, and consensus promotor logos were derived. Interestingly, many leaderless messenger RNAs (mRNAs) were found. In addition, many mRNAs were transcribed from multiple alternative TSSs. We observed pervasive intragenic TSSs both in sense and antisense to CDSs. Antisense transcripts were enriched near the 5′ end of mRNAs, indicating a functional role in post‐transcriptional regulation. In total, 578 TSSs were detected in intergenic regions, of which 35 were identified as putative small regulatory RNAs. Finally, we provide a detailed analysis of the main copper resistance clusters in CH34, which include many intragenic and antisense transcripts. These results clearly highlight the ubiquity of noncoding transcripts in the CH34 transcriptome, many of which are putatively involved in the regulation of metal resistance.

KW - Copper

KW - Cupriavidus metallidurans

KW - Differential gene expression

KW - Differential RNA‐sequencing

KW - Gene regulation

KW - SRNA

KW - Transcription start site

UR - https://www.scopus.com/pages/publications/85090733506

U2 - 10.3390/genes11091049

DO - 10.3390/genes11091049

M3 - Article

C2 - 32899882

AN - SCOPUS:85090733506

VL - 11

SP - 1

EP - 24

JO - Genes

JF - Genes

IS - 9

M1 - 1049

ER -

The transcriptomic landscape of cupriavidus metallidurans CH34 acutely exposed to copper

Abstract

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Keywords

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