ChlR protein of Synechococcus sp. PCC 7002 is a transcription activator that uses an oxygen-sensitive [4Fe-4S] cluster to control genes involved in pigment biosynthesis

Marcus Ludwig, Maria Eirini Pandelia, Chyue Yie Chew, Bo Zhang, John H. Golbeck, Carsten Krebs, Donald Ashley Bryant

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Synechococcus sp. PCC 7002 and many other cyanobacteria have two genes that encode key enzymes involved in chlorophyll a, biliverdin, and heme biosynthesis: acsFI/acsFII, ho1/ho2, and hemF/hemN. Under atmospheric O2 levels, AcsFI synthesizes 3,8-divinyl protochlorophyllide from Mg-protoporphyrin IX monomethyl ester, Ho1 oxidatively cleaves heme to form biliverdin, and HemF oxidizes coproporphyrinogen III to protoporphyrinogen IX. Under microoxic conditions, another set of genes directs the synthesis of alternative enzymes AcsFII, Ho2, and HemN. In Synechococcus sp. PCC 7002, open reading frame SynPCC7002-A1993 encodes a MarR family transcriptional regulator, which is located immediately upstream from the operon comprising acsFII, ho2, hemN, and desF (the latter encodes a putative fatty acid desaturase). Deletion and complementation analyses showed that this gene, denoted chlR, is a transcriptional activator that is essential for transcription of the acsFII-ho2-hemN-desF operon under microoxic conditions. Global transcriptome analyses showed that ChlR controls the expression of only these four genes. Co-expression of chlR with a yfp reporter gene under the control of the acsFII promoter from Synechocystis sp. PCC 6803 in Escherichia coli demonstrated that no other cyanobacterium-specific components are required for proper functioning of this regulatory circuit. A combination of analytical methods and Mössbauer and EPR spectroscopies showed that reconstituted, recombinant ChlR forms homodimers that harbor one oxygen-sensitive [4Fe-4S] cluster. We conclude that ChlR is a transcriptional activator that uses a [4Fe-4S] cluster to sense O2 levels and thereby control the expression of the acsFII-ho2-hemN-desF operon.

Original languageEnglish (US)
Pages (from-to)16624-16639
Number of pages16
JournalJournal of Biological Chemistry
Volume289
Issue number24
DOIs
StatePublished - Jun 13 2014

Fingerprint

Synechococcus
Biosynthesis
Transcription
Pigments
Operon
Genes
Biliverdine
Oxygen
Cyanobacteria
Heme
Proteins
Fatty Acid Desaturases
Synechocystis
Gene Expression Profiling
Enzymes
Reporter Genes
Open Reading Frames
Spectrum Analysis
Ports and harbors
Escherichia coli

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

@article{2e884559ecb54e3b822e7cd61fdc06f1,
title = "ChlR protein of Synechococcus sp. PCC 7002 is a transcription activator that uses an oxygen-sensitive [4Fe-4S] cluster to control genes involved in pigment biosynthesis",
abstract = "Synechococcus sp. PCC 7002 and many other cyanobacteria have two genes that encode key enzymes involved in chlorophyll a, biliverdin, and heme biosynthesis: acsFI/acsFII, ho1/ho2, and hemF/hemN. Under atmospheric O2 levels, AcsFI synthesizes 3,8-divinyl protochlorophyllide from Mg-protoporphyrin IX monomethyl ester, Ho1 oxidatively cleaves heme to form biliverdin, and HemF oxidizes coproporphyrinogen III to protoporphyrinogen IX. Under microoxic conditions, another set of genes directs the synthesis of alternative enzymes AcsFII, Ho2, and HemN. In Synechococcus sp. PCC 7002, open reading frame SynPCC7002-A1993 encodes a MarR family transcriptional regulator, which is located immediately upstream from the operon comprising acsFII, ho2, hemN, and desF (the latter encodes a putative fatty acid desaturase). Deletion and complementation analyses showed that this gene, denoted chlR, is a transcriptional activator that is essential for transcription of the acsFII-ho2-hemN-desF operon under microoxic conditions. Global transcriptome analyses showed that ChlR controls the expression of only these four genes. Co-expression of chlR with a yfp reporter gene under the control of the acsFII promoter from Synechocystis sp. PCC 6803 in Escherichia coli demonstrated that no other cyanobacterium-specific components are required for proper functioning of this regulatory circuit. A combination of analytical methods and M{\"o}ssbauer and EPR spectroscopies showed that reconstituted, recombinant ChlR forms homodimers that harbor one oxygen-sensitive [4Fe-4S] cluster. We conclude that ChlR is a transcriptional activator that uses a [4Fe-4S] cluster to sense O2 levels and thereby control the expression of the acsFII-ho2-hemN-desF operon.",
author = "Marcus Ludwig and Pandelia, {Maria Eirini} and Chew, {Chyue Yie} and Bo Zhang and Golbeck, {John H.} and Carsten Krebs and Bryant, {Donald Ashley}",
year = "2014",
month = "6",
day = "13",
doi = "10.1074/jbc.M114.561233",
language = "English (US)",
volume = "289",
pages = "16624--16639",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "24",

}

ChlR protein of Synechococcus sp. PCC 7002 is a transcription activator that uses an oxygen-sensitive [4Fe-4S] cluster to control genes involved in pigment biosynthesis. / Ludwig, Marcus; Pandelia, Maria Eirini; Chew, Chyue Yie; Zhang, Bo; Golbeck, John H.; Krebs, Carsten; Bryant, Donald Ashley.

In: Journal of Biological Chemistry, Vol. 289, No. 24, 13.06.2014, p. 16624-16639.

Research output: Contribution to journalArticle

TY - JOUR

T1 - ChlR protein of Synechococcus sp. PCC 7002 is a transcription activator that uses an oxygen-sensitive [4Fe-4S] cluster to control genes involved in pigment biosynthesis

AU - Ludwig, Marcus

AU - Pandelia, Maria Eirini

AU - Chew, Chyue Yie

AU - Zhang, Bo

AU - Golbeck, John H.

AU - Krebs, Carsten

AU - Bryant, Donald Ashley

PY - 2014/6/13

Y1 - 2014/6/13

N2 - Synechococcus sp. PCC 7002 and many other cyanobacteria have two genes that encode key enzymes involved in chlorophyll a, biliverdin, and heme biosynthesis: acsFI/acsFII, ho1/ho2, and hemF/hemN. Under atmospheric O2 levels, AcsFI synthesizes 3,8-divinyl protochlorophyllide from Mg-protoporphyrin IX monomethyl ester, Ho1 oxidatively cleaves heme to form biliverdin, and HemF oxidizes coproporphyrinogen III to protoporphyrinogen IX. Under microoxic conditions, another set of genes directs the synthesis of alternative enzymes AcsFII, Ho2, and HemN. In Synechococcus sp. PCC 7002, open reading frame SynPCC7002-A1993 encodes a MarR family transcriptional regulator, which is located immediately upstream from the operon comprising acsFII, ho2, hemN, and desF (the latter encodes a putative fatty acid desaturase). Deletion and complementation analyses showed that this gene, denoted chlR, is a transcriptional activator that is essential for transcription of the acsFII-ho2-hemN-desF operon under microoxic conditions. Global transcriptome analyses showed that ChlR controls the expression of only these four genes. Co-expression of chlR with a yfp reporter gene under the control of the acsFII promoter from Synechocystis sp. PCC 6803 in Escherichia coli demonstrated that no other cyanobacterium-specific components are required for proper functioning of this regulatory circuit. A combination of analytical methods and Mössbauer and EPR spectroscopies showed that reconstituted, recombinant ChlR forms homodimers that harbor one oxygen-sensitive [4Fe-4S] cluster. We conclude that ChlR is a transcriptional activator that uses a [4Fe-4S] cluster to sense O2 levels and thereby control the expression of the acsFII-ho2-hemN-desF operon.

AB - Synechococcus sp. PCC 7002 and many other cyanobacteria have two genes that encode key enzymes involved in chlorophyll a, biliverdin, and heme biosynthesis: acsFI/acsFII, ho1/ho2, and hemF/hemN. Under atmospheric O2 levels, AcsFI synthesizes 3,8-divinyl protochlorophyllide from Mg-protoporphyrin IX monomethyl ester, Ho1 oxidatively cleaves heme to form biliverdin, and HemF oxidizes coproporphyrinogen III to protoporphyrinogen IX. Under microoxic conditions, another set of genes directs the synthesis of alternative enzymes AcsFII, Ho2, and HemN. In Synechococcus sp. PCC 7002, open reading frame SynPCC7002-A1993 encodes a MarR family transcriptional regulator, which is located immediately upstream from the operon comprising acsFII, ho2, hemN, and desF (the latter encodes a putative fatty acid desaturase). Deletion and complementation analyses showed that this gene, denoted chlR, is a transcriptional activator that is essential for transcription of the acsFII-ho2-hemN-desF operon under microoxic conditions. Global transcriptome analyses showed that ChlR controls the expression of only these four genes. Co-expression of chlR with a yfp reporter gene under the control of the acsFII promoter from Synechocystis sp. PCC 6803 in Escherichia coli demonstrated that no other cyanobacterium-specific components are required for proper functioning of this regulatory circuit. A combination of analytical methods and Mössbauer and EPR spectroscopies showed that reconstituted, recombinant ChlR forms homodimers that harbor one oxygen-sensitive [4Fe-4S] cluster. We conclude that ChlR is a transcriptional activator that uses a [4Fe-4S] cluster to sense O2 levels and thereby control the expression of the acsFII-ho2-hemN-desF operon.

UR - http://www.scopus.com/inward/record.url?scp=84902440208&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84902440208&partnerID=8YFLogxK

U2 - 10.1074/jbc.M114.561233

DO - 10.1074/jbc.M114.561233

M3 - Article

C2 - 24782315

AN - SCOPUS:84902440208

VL - 289

SP - 16624

EP - 16639

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 24

ER -