An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum

Pectobacterium carotovorum is an important plant pathogen responsible for the destruction of crops through bacterial soft rot, which is modulated by oxygen (O2) concentration. A soluble globin coupled sensor protein, Pcc DgcO (also referred to as PccGCS) is one way through which P. carotovorum sense...

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Main Authors: Florian J. Fekete, Nick J. Marotta, Xuanyu Liu, Emily E. Weinert
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1134742/full
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author Florian J. Fekete
Nick J. Marotta
Xuanyu Liu
Emily E. Weinert
Emily E. Weinert
author_facet Florian J. Fekete
Nick J. Marotta
Xuanyu Liu
Emily E. Weinert
Emily E. Weinert
author_sort Florian J. Fekete
collection DOAJ
description Pectobacterium carotovorum is an important plant pathogen responsible for the destruction of crops through bacterial soft rot, which is modulated by oxygen (O2) concentration. A soluble globin coupled sensor protein, Pcc DgcO (also referred to as PccGCS) is one way through which P. carotovorum senses oxygen. DgcO contains a diguanylate cyclase output domain producing c-di-GMP. Synthesis of the bacterial second messenger c-di-GMP is increased upon oxygen binding to the sensory globin domain. This work seeks to understand regulation of function by DgcO at the transcript level. RNA sequencing and differential expression analysis revealed that the deletion of DgcO only affects transcript levels in cells grown under aerobic conditions. Differential expression analysis showed that DgcO deletion alters transcript levels for metal transporters. These results, followed by inductively coupled plasma—mass spectrometry showing decreased concentrations of six biologically relevant metals upon DgcO deletion, provide evidence that a globin coupled sensor can affect cellular metal content. These findings improve the understanding of the transcript level control of O2-dependent phenotypes in an important phytopathogen and establish a basis for further studies on c-di-GMP-dependent functions in P. carotovorum.
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spelling doaj.art-49d9a14bd29342f98b190e633b8648cc2023-07-07T12:54:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-07-011410.3389/fmicb.2023.11347421134742An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorumFlorian J. Fekete0Nick J. Marotta1Xuanyu Liu2Emily E. Weinert3Emily E. Weinert4Department of Biochemistry and Molecular Biology, Penn State University, University Park, PA, United StatesGraduate Program in Molecular, Cellular, and Integrative Biosciences, Penn State University, University Park, PA, United StatesDepartment of Biochemistry and Molecular Biology, Penn State University, University Park, PA, United StatesDepartment of Biochemistry and Molecular Biology, Penn State University, University Park, PA, United StatesDepartment of Chemistry, Penn State University, University Park, PA, United StatesPectobacterium carotovorum is an important plant pathogen responsible for the destruction of crops through bacterial soft rot, which is modulated by oxygen (O2) concentration. A soluble globin coupled sensor protein, Pcc DgcO (also referred to as PccGCS) is one way through which P. carotovorum senses oxygen. DgcO contains a diguanylate cyclase output domain producing c-di-GMP. Synthesis of the bacterial second messenger c-di-GMP is increased upon oxygen binding to the sensory globin domain. This work seeks to understand regulation of function by DgcO at the transcript level. RNA sequencing and differential expression analysis revealed that the deletion of DgcO only affects transcript levels in cells grown under aerobic conditions. Differential expression analysis showed that DgcO deletion alters transcript levels for metal transporters. These results, followed by inductively coupled plasma—mass spectrometry showing decreased concentrations of six biologically relevant metals upon DgcO deletion, provide evidence that a globin coupled sensor can affect cellular metal content. These findings improve the understanding of the transcript level control of O2-dependent phenotypes in an important phytopathogen and establish a basis for further studies on c-di-GMP-dependent functions in P. carotovorum.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1134742/fullcyclic-di-GMPoxygenPectobacteriumglobindiguanylate cyclase
spellingShingle Florian J. Fekete
Nick J. Marotta
Xuanyu Liu
Emily E. Weinert
Emily E. Weinert
An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum
Frontiers in Microbiology
cyclic-di-GMP
oxygen
Pectobacterium
globin
diguanylate cyclase
title An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum
title_full An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum
title_fullStr An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum
title_full_unstemmed An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum
title_short An O2-sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen Pectobacterium carotovorum
title_sort o2 sensing diguanylate cyclase broadly affects the aerobic transcriptome in the phytopathogen pectobacterium carotovorum
topic cyclic-di-GMP
oxygen
Pectobacterium
globin
diguanylate cyclase
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1134742/full
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