Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis

ABSTRACT The precursors of the diffusible signal factor (DSF) family signals of Xanthomonas campestris pv. campestris are 3-hydroxyacyl-acyl carrier protein (3-hydroxyacyl-ACP) thioesters having acyl chains of 12 to 13 carbon atoms produced by the fatty acid biosynthetic pathway. We report a novel 3...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Zhe Hu, Huijuan Dong, Jin-Cheng Ma, Yonghong Yu, Kai-Hui Li, Qiao-Qiao Guo, Chao Zhang, Wen-Bin Zhang, Xinyun Cao, John E. Cronan, Haihong Wang
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://doaj.org/article/10fd44b34fac497097a72dcacbc6126c
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:10fd44b34fac497097a72dcacbc6126c
record_format dspace
spelling oai:doaj.org-article:10fd44b34fac497097a72dcacbc6126c2021-11-15T16:00:24ZNovel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis10.1128/mBio.00596-182150-7511https://doaj.org/article/10fd44b34fac497097a72dcacbc6126c2018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00596-18https://doaj.org/toc/2150-7511ABSTRACT The precursors of the diffusible signal factor (DSF) family signals of Xanthomonas campestris pv. campestris are 3-hydroxyacyl-acyl carrier protein (3-hydroxyacyl-ACP) thioesters having acyl chains of 12 to 13 carbon atoms produced by the fatty acid biosynthetic pathway. We report a novel 3-oxoacyl-ACP reductase encoded by the X. campestris pv. campestris XCC0416 gene (fabG2), which is unable to participate in the initial steps of fatty acyl synthesis. This was shown by the failure of FabG2 expression to allow growth at the nonpermissive temperature of an Escherichia coli fabG temperature-sensitive strain. However, when transformed into the E. coli strain together with a plasmid bearing the Vibrio harveyi acyl-ACP synthetase gene (aasS), growth proceeded, but only when the medium contained octanoic acid. In vitro assays showed that FabG2 catalyzes the reduction of long-chain (≥C8) 3-oxoacyl-ACPs to 3-hydroxyacyl-ACPs but is only weakly active with shorter-chain (C4, C6) substrates. FabG1, the housekeeping 3-oxoacyl-ACP reductase encoded within the fatty acid synthesis gene cluster, could be deleted in a strain that overexpressed fabG2 but only in octanoic acid-supplemented media. Growth of the X. campestris pv. campestris ΔfabG1 strain overexpressing fabG2 required fabH for growth with octanoic acid, indicating that octanoyl coenzyme A is elongated by X. campestris pv. campestris fabH. Deletion of fabG2 reduced DSF family signal production, whereas overproduction of either FabG1 or FabG2 in the ΔfabG2 strain restored DSF family signal levels. IMPORTANCE Quorum sensing mediated by DSF signaling molecules regulates pathogenesis in several different phytopathogenic bacteria, including Xanthomonas campestris pv. campestris. DSF signaling also plays a key role in infection by the human pathogen Burkholderia cepacia. The acyl chains of the DSF molecules are diverted and remodeled from a key intermediate of the fatty acid synthesis pathway. We report a Xanthomonas campestris pv. campestris fatty acid synthesis enzyme, FabG2, of novel specificity that seems tailored to provide DSF signaling molecule precursors.Zhe HuHuijuan DongJin-Cheng MaYonghong YuKai-Hui LiQiao-Qiao GuoChao ZhangWen-Bin ZhangXinyun CaoJohn E. CronanHaihong WangAmerican Society for MicrobiologyarticleXanthomonasfatty acidsquorum sensingMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic Xanthomonas
fatty acids
quorum sensing
Microbiology
QR1-502
spellingShingle Xanthomonas
fatty acids
quorum sensing
Microbiology
QR1-502
Zhe Hu
Huijuan Dong
Jin-Cheng Ma
Yonghong Yu
Kai-Hui Li
Qiao-Qiao Guo
Chao Zhang
Wen-Bin Zhang
Xinyun Cao
John E. Cronan
Haihong Wang
Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis
description ABSTRACT The precursors of the diffusible signal factor (DSF) family signals of Xanthomonas campestris pv. campestris are 3-hydroxyacyl-acyl carrier protein (3-hydroxyacyl-ACP) thioesters having acyl chains of 12 to 13 carbon atoms produced by the fatty acid biosynthetic pathway. We report a novel 3-oxoacyl-ACP reductase encoded by the X. campestris pv. campestris XCC0416 gene (fabG2), which is unable to participate in the initial steps of fatty acyl synthesis. This was shown by the failure of FabG2 expression to allow growth at the nonpermissive temperature of an Escherichia coli fabG temperature-sensitive strain. However, when transformed into the E. coli strain together with a plasmid bearing the Vibrio harveyi acyl-ACP synthetase gene (aasS), growth proceeded, but only when the medium contained octanoic acid. In vitro assays showed that FabG2 catalyzes the reduction of long-chain (≥C8) 3-oxoacyl-ACPs to 3-hydroxyacyl-ACPs but is only weakly active with shorter-chain (C4, C6) substrates. FabG1, the housekeeping 3-oxoacyl-ACP reductase encoded within the fatty acid synthesis gene cluster, could be deleted in a strain that overexpressed fabG2 but only in octanoic acid-supplemented media. Growth of the X. campestris pv. campestris ΔfabG1 strain overexpressing fabG2 required fabH for growth with octanoic acid, indicating that octanoyl coenzyme A is elongated by X. campestris pv. campestris fabH. Deletion of fabG2 reduced DSF family signal production, whereas overproduction of either FabG1 or FabG2 in the ΔfabG2 strain restored DSF family signal levels. IMPORTANCE Quorum sensing mediated by DSF signaling molecules regulates pathogenesis in several different phytopathogenic bacteria, including Xanthomonas campestris pv. campestris. DSF signaling also plays a key role in infection by the human pathogen Burkholderia cepacia. The acyl chains of the DSF molecules are diverted and remodeled from a key intermediate of the fatty acid synthesis pathway. We report a Xanthomonas campestris pv. campestris fatty acid synthesis enzyme, FabG2, of novel specificity that seems tailored to provide DSF signaling molecule precursors.
format article
author Zhe Hu
Huijuan Dong
Jin-Cheng Ma
Yonghong Yu
Kai-Hui Li
Qiao-Qiao Guo
Chao Zhang
Wen-Bin Zhang
Xinyun Cao
John E. Cronan
Haihong Wang
author_facet Zhe Hu
Huijuan Dong
Jin-Cheng Ma
Yonghong Yu
Kai-Hui Li
Qiao-Qiao Guo
Chao Zhang
Wen-Bin Zhang
Xinyun Cao
John E. Cronan
Haihong Wang
author_sort Zhe Hu
title Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis
title_short Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis
title_full Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis
title_fullStr Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis
title_full_unstemmed Novel <named-content content-type="genus-species">Xanthomonas campestris</named-content> Long-Chain-Specific 3-Oxoacyl-Acyl Carrier Protein Reductase Involved in Diffusible Signal Factor Synthesis
title_sort novel <named-content content-type="genus-species">xanthomonas campestris</named-content> long-chain-specific 3-oxoacyl-acyl carrier protein reductase involved in diffusible signal factor synthesis
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/10fd44b34fac497097a72dcacbc6126c
work_keys_str_mv AT zhehu novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT huijuandong novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT jinchengma novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT yonghongyu novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT kaihuili novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT qiaoqiaoguo novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT chaozhang novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT wenbinzhang novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT xinyuncao novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT johnecronan novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
AT haihongwang novelnamedcontentcontenttypegenusspeciesxanthomonascampestrisnamedcontentlongchainspecific3oxoacylacylcarrierproteinreductaseinvolvedindiffusiblesignalfactorsynthesis
_version_ 1718426948914380800