Cargando…

Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis

Toxin–antitoxin (TA) systems are prevalent in bacteria and archaea. However, related studies in the ecologically and bioelectrochemically important strain Shewanella oneidensis are limited. Here, we show that SO_3166, a member of the higher eukaryotes and prokaryotes nucleotide-binding (HEPN) superf...

Descripción completa

Detalles Bibliográficos
Autores principales: Yao, Jianyun, Guo, Yunxue, Zeng, Zhenshun, Liu, Xiaoxiao, Shi, Fei, Wang, Xiaoxue
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Ltd 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4621449/
https://www.ncbi.nlm.nih.gov/pubmed/26112399
http://dx.doi.org/10.1111/1751-7915.12294
_version_ 1782397445382078464
author Yao, Jianyun
Guo, Yunxue
Zeng, Zhenshun
Liu, Xiaoxiao
Shi, Fei
Wang, Xiaoxue
author_facet Yao, Jianyun
Guo, Yunxue
Zeng, Zhenshun
Liu, Xiaoxiao
Shi, Fei
Wang, Xiaoxue
author_sort Yao, Jianyun
collection PubMed
description Toxin–antitoxin (TA) systems are prevalent in bacteria and archaea. However, related studies in the ecologically and bioelectrochemically important strain Shewanella oneidensis are limited. Here, we show that SO_3166, a member of the higher eukaryotes and prokaryotes nucleotide-binding (HEPN) superfamily, strongly inhibited cell growth in S. oneidensis and Escherichia coli. SO_3165, a putative minimal nucleotidyltransferase (MNT), neutralized the toxicity of SO_3166. Gene SO_3165 lies upstream of SO_3166, and they are co-transcribed. Moreover, the SO_3165 and SO_3166 proteins interact with each other directly in vivo, and antitoxin SO_3165 bound to the promoter of the TA operon and repressed its activity. Finally, the conserved Rx4-6H domain in HEPN family was identified in SO_3166. Mutating either the R or H abolished SO_3166 toxicity, confirming that Rx4-6H domain is critical for SO_3166 activity. Taken together, these results demonstrate that SO_3166 and SO_3165 in S. oneidensis form a typical type II TA pair. This TA pair plays a critical role in regulating bacterial functions because its disruption led to impaired cell motility in S. oneidensis. Thus, we demonstrated for the first time that HEPN-MNT can function as a TA system, thereby providing important insights into the understanding of the function and regulation of HEPNs and MNTs in prokaryotes.
format Online
Article
Text
id pubmed-4621449
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher John Wiley & Sons, Ltd
record_format MEDLINE/PubMed
spelling pubmed-46214492015-10-30 Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis Yao, Jianyun Guo, Yunxue Zeng, Zhenshun Liu, Xiaoxiao Shi, Fei Wang, Xiaoxue Microb Biotechnol Research Articles Toxin–antitoxin (TA) systems are prevalent in bacteria and archaea. However, related studies in the ecologically and bioelectrochemically important strain Shewanella oneidensis are limited. Here, we show that SO_3166, a member of the higher eukaryotes and prokaryotes nucleotide-binding (HEPN) superfamily, strongly inhibited cell growth in S. oneidensis and Escherichia coli. SO_3165, a putative minimal nucleotidyltransferase (MNT), neutralized the toxicity of SO_3166. Gene SO_3165 lies upstream of SO_3166, and they are co-transcribed. Moreover, the SO_3165 and SO_3166 proteins interact with each other directly in vivo, and antitoxin SO_3165 bound to the promoter of the TA operon and repressed its activity. Finally, the conserved Rx4-6H domain in HEPN family was identified in SO_3166. Mutating either the R or H abolished SO_3166 toxicity, confirming that Rx4-6H domain is critical for SO_3166 activity. Taken together, these results demonstrate that SO_3166 and SO_3165 in S. oneidensis form a typical type II TA pair. This TA pair plays a critical role in regulating bacterial functions because its disruption led to impaired cell motility in S. oneidensis. Thus, we demonstrated for the first time that HEPN-MNT can function as a TA system, thereby providing important insights into the understanding of the function and regulation of HEPNs and MNTs in prokaryotes. John Wiley & Sons, Ltd 2015-09 2015-06-25 /pmc/articles/PMC4621449/ /pubmed/26112399 http://dx.doi.org/10.1111/1751-7915.12294 Text en Journal compilation © 2015 John Wiley & Sons Ltd and Society for Applied Microbiology http://creativecommons.org/licenses/by/4.0/ This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Yao, Jianyun
Guo, Yunxue
Zeng, Zhenshun
Liu, Xiaoxiao
Shi, Fei
Wang, Xiaoxue
Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis
title Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis
title_full Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis
title_fullStr Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis
title_full_unstemmed Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis
title_short Identification and characterization of a HEPN-MNT family type II toxin–antitoxin in Shewanella oneidensis
title_sort identification and characterization of a hepn-mnt family type ii toxin–antitoxin in shewanella oneidensis
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4621449/
https://www.ncbi.nlm.nih.gov/pubmed/26112399
http://dx.doi.org/10.1111/1751-7915.12294
work_keys_str_mv AT yaojianyun identificationandcharacterizationofahepnmntfamilytypeiitoxinantitoxininshewanellaoneidensis
AT guoyunxue identificationandcharacterizationofahepnmntfamilytypeiitoxinantitoxininshewanellaoneidensis
AT zengzhenshun identificationandcharacterizationofahepnmntfamilytypeiitoxinantitoxininshewanellaoneidensis
AT liuxiaoxiao identificationandcharacterizationofahepnmntfamilytypeiitoxinantitoxininshewanellaoneidensis
AT shifei identificationandcharacterizationofahepnmntfamilytypeiitoxinantitoxininshewanellaoneidensis
AT wangxiaoxue identificationandcharacterizationofahepnmntfamilytypeiitoxinantitoxininshewanellaoneidensis