A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>

ABSTRACT Zeamines are a family of polyamino phytotoxins produced by Dickeya zeae EC1. These phytotoxins are also potent antibiotics against a range of microorganisms. To understand how D. zeae EC1 can protect itself from the antimicrobial activity of zeamines, we tested whether the ABC transporter g...

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Autores principales:	Zhibin Liang, Luhao Huang, Fei He, Xiaofan Zhou, Zurong Shi, Jianuan Zhou, Yufan Chen, Mingfa Lv, Yumei Chen, Lian-Hui Zhang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	RND efflux pump antimicrobial resistance phytotoxin rice stem rot zeamines Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/55e0b9ceb61946fd9f9fd15e4794d68a
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spelling	oai:doaj.org-article:55e0b9ceb61946fd9f9fd15e4794d68a2021-11-15T15:55:25ZA Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>10.1128/mBio.00713-192150-7511https://doaj.org/article/55e0b9ceb61946fd9f9fd15e4794d68a2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00713-19https://doaj.org/toc/2150-7511ABSTRACT Zeamines are a family of polyamino phytotoxins produced by Dickeya zeae EC1. These phytotoxins are also potent antibiotics against a range of microorganisms. To understand how D. zeae EC1 can protect itself from the antimicrobial activity of zeamines, we tested whether the ABC transporter genes within the zms (zeamine synthesis) gene cluster were related to zeamine resistance. Our results ruled out the possible involvement of these ABC transporters in zeamine resistance and instead unveiled an RND (resistance-nodulation-cell division) efflux pump, DesABC, which plays an important role in zeamine resistance in D. zeae EC1. The desAB genes are located next to the zms gene cluster, but desC is at a distant location in the bacterial genome. Null mutation of the desABC genes in a zeamine-minus derivative of strain EC1 led to about an 8- to 32-fold decrease in zeamine tolerance level. This efflux pump was zeamine specific and appeared to be conserved only in Dickeya species, which may explain the high potency of zeamines against a wide range of bacterial pathogens. Significantly, expression of the desAB genes was abolished by deletion of zmsA, which encodes zeamine biosynthesis but could be induced by exogenous addition of zeamines. The results suggest that sophisticated and coordinated regulatory mechanisms have evolved to govern zeamine production and tolerance. Taken together, these findings documented a novel signaling role of zeamines and the first resistance mechanism against zeamines, which is a family of potent and promising antibiotics against both Gram-positive and Gram-negative bacterial pathogens. IMPORTANCE Zeamines are a family of newly identified phytotoxins and potent antibiotics produced by D. zeae EC1. Unlike most bacterial organisms, which are highly sensitive, D. zeae EC1 is tolerant to zeamines, but the mechanisms involved are unknown. Our study showed, for the first time, that a new RND efflux pump, DesABC, is indispensable for D. zeae EC1 against zeamines. We found that the DesABC efflux pump was zeamine specific and appeared to be conserved only in the Dickeya species, which may explain the high potency of zeamines against a wide range of bacterial pathogens. We also showed that expression of DesABC efflux system genes was induced by zeamines. These findings not only provide an answer to why D. zeae EC1 is much more tolerant to zeamines than other bacterial pathogens but also document a signaling role of zeamines in modulation of gene expression.Zhibin LiangLuhao HuangFei HeXiaofan ZhouZurong ShiJianuan ZhouYufan ChenMingfa LvYumei ChenLian-Hui ZhangAmerican Society for MicrobiologyarticleRND efflux pumpantimicrobial resistancephytotoxinrice stem rotzeaminesMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	RND efflux pump antimicrobial resistance phytotoxin rice stem rot zeamines Microbiology QR1-502
spellingShingle	RND efflux pump antimicrobial resistance phytotoxin rice stem rot zeamines Microbiology QR1-502 Zhibin Liang Luhao Huang Fei He Xiaofan Zhou Zurong Shi Jianuan Zhou Yufan Chen Mingfa Lv Yumei Chen Lian-Hui Zhang A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>
description	ABSTRACT Zeamines are a family of polyamino phytotoxins produced by Dickeya zeae EC1. These phytotoxins are also potent antibiotics against a range of microorganisms. To understand how D. zeae EC1 can protect itself from the antimicrobial activity of zeamines, we tested whether the ABC transporter genes within the zms (zeamine synthesis) gene cluster were related to zeamine resistance. Our results ruled out the possible involvement of these ABC transporters in zeamine resistance and instead unveiled an RND (resistance-nodulation-cell division) efflux pump, DesABC, which plays an important role in zeamine resistance in D. zeae EC1. The desAB genes are located next to the zms gene cluster, but desC is at a distant location in the bacterial genome. Null mutation of the desABC genes in a zeamine-minus derivative of strain EC1 led to about an 8- to 32-fold decrease in zeamine tolerance level. This efflux pump was zeamine specific and appeared to be conserved only in Dickeya species, which may explain the high potency of zeamines against a wide range of bacterial pathogens. Significantly, expression of the desAB genes was abolished by deletion of zmsA, which encodes zeamine biosynthesis but could be induced by exogenous addition of zeamines. The results suggest that sophisticated and coordinated regulatory mechanisms have evolved to govern zeamine production and tolerance. Taken together, these findings documented a novel signaling role of zeamines and the first resistance mechanism against zeamines, which is a family of potent and promising antibiotics against both Gram-positive and Gram-negative bacterial pathogens. IMPORTANCE Zeamines are a family of newly identified phytotoxins and potent antibiotics produced by D. zeae EC1. Unlike most bacterial organisms, which are highly sensitive, D. zeae EC1 is tolerant to zeamines, but the mechanisms involved are unknown. Our study showed, for the first time, that a new RND efflux pump, DesABC, is indispensable for D. zeae EC1 against zeamines. We found that the DesABC efflux pump was zeamine specific and appeared to be conserved only in the Dickeya species, which may explain the high potency of zeamines against a wide range of bacterial pathogens. We also showed that expression of DesABC efflux system genes was induced by zeamines. These findings not only provide an answer to why D. zeae EC1 is much more tolerant to zeamines than other bacterial pathogens but also document a signaling role of zeamines in modulation of gene expression.
format	article
author	Zhibin Liang Luhao Huang Fei He Xiaofan Zhou Zurong Shi Jianuan Zhou Yufan Chen Mingfa Lv Yumei Chen Lian-Hui Zhang
author_facet	Zhibin Liang Luhao Huang Fei He Xiaofan Zhou Zurong Shi Jianuan Zhou Yufan Chen Mingfa Lv Yumei Chen Lian-Hui Zhang
author_sort	Zhibin Liang
title	A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>
title_short	A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>
title_full	A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>
title_fullStr	A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>
title_full_unstemmed	A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>
title_sort	substrate-activated efflux pump, desabc, confers zeamine resistance to <named-content content-type="genus-species">dickeya zeae</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/55e0b9ceb61946fd9f9fd15e4794d68a
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A Substrate-Activated Efflux Pump, DesABC, Confers Zeamine Resistance to <named-content content-type="genus-species">Dickeya zeae</named-content>

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