Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon

The orange carotenoid protein (OCP) family of proteins are light-activated proteins that function in dissipating excess energy absorbed by accessory light-harvesting complexes, i.e., phycobilisomes (PBSs), in cyanobacteria. Some cyanobacteria contain multiple homologs of the OCP-encoding gene (ocp)....

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Main Authors: D. Isabel Petrescu, Preston L. Dilbeck, Beronda L. Montgomery
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.819604/full
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author D. Isabel Petrescu
D. Isabel Petrescu
Preston L. Dilbeck
Beronda L. Montgomery
Beronda L. Montgomery
Beronda L. Montgomery
author_facet D. Isabel Petrescu
D. Isabel Petrescu
Preston L. Dilbeck
Beronda L. Montgomery
Beronda L. Montgomery
Beronda L. Montgomery
author_sort D. Isabel Petrescu
collection DOAJ
description The orange carotenoid protein (OCP) family of proteins are light-activated proteins that function in dissipating excess energy absorbed by accessory light-harvesting complexes, i.e., phycobilisomes (PBSs), in cyanobacteria. Some cyanobacteria contain multiple homologs of the OCP-encoding gene (ocp). Fremyella diplosiphon, a cyanobacterium studied for light-dependent regulation of PBSs during complementary chromatic acclimation (CCA), contains several OCP homologs – two full-length OCPs, three Helical Carotenoid Proteins (HCPs) with homology to the N-terminus of OCP, and one C-terminal domain-like carotenoid protein (CCP) with homology to the C-terminus of OCP. We examined whether these homologs are distinctly regulated in response to different environmental factors, which could indicate distinct functions. We observed distinct patterns of expression for some OCP, HCP, and CCP encoding genes, and have evidence that light-dependent aspects of ocp homolog expression are regulated by photoreceptor RcaE which controls CCA. RcaE-dependent transcriptional regulator RcaC is also involved in the photoregulation of some hcp genes. Apart from light, additional environmental factors associated with cellular redox regulation impact the mRNA levels of ocp homologs, including salt, cold, and disruption of electron transport. Analyses of conserved sequences in the promoters of ocp homologs were conducted to gain additional insight into regulation of these genes. Several conserved regulatory elements were found across multiple ocp homolog promoters that potentially control differential transcriptional regulation in response to a range of environmental cues. The impact of distinct environmental cues on differential accumulation of ocp homolog transcripts indicates potential functional diversification of this gene family in cyanobacteria. These genes likely enable dynamic cellular protection in response to diverse environmental stress conditions in F. diplosiphon.
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spelling doaj.art-0de541bd08ce48508a93e89d6356435a2022-12-21T19:39:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-12-011210.3389/fmicb.2021.819604819604Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphonD. Isabel Petrescu0D. Isabel Petrescu1Preston L. Dilbeck2Beronda L. Montgomery3Beronda L. Montgomery4Beronda L. Montgomery5MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United StatesMSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, United StatesMSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, United StatesDepartment of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, United StatesDepartment of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI, United StatesThe orange carotenoid protein (OCP) family of proteins are light-activated proteins that function in dissipating excess energy absorbed by accessory light-harvesting complexes, i.e., phycobilisomes (PBSs), in cyanobacteria. Some cyanobacteria contain multiple homologs of the OCP-encoding gene (ocp). Fremyella diplosiphon, a cyanobacterium studied for light-dependent regulation of PBSs during complementary chromatic acclimation (CCA), contains several OCP homologs – two full-length OCPs, three Helical Carotenoid Proteins (HCPs) with homology to the N-terminus of OCP, and one C-terminal domain-like carotenoid protein (CCP) with homology to the C-terminus of OCP. We examined whether these homologs are distinctly regulated in response to different environmental factors, which could indicate distinct functions. We observed distinct patterns of expression for some OCP, HCP, and CCP encoding genes, and have evidence that light-dependent aspects of ocp homolog expression are regulated by photoreceptor RcaE which controls CCA. RcaE-dependent transcriptional regulator RcaC is also involved in the photoregulation of some hcp genes. Apart from light, additional environmental factors associated with cellular redox regulation impact the mRNA levels of ocp homologs, including salt, cold, and disruption of electron transport. Analyses of conserved sequences in the promoters of ocp homologs were conducted to gain additional insight into regulation of these genes. Several conserved regulatory elements were found across multiple ocp homolog promoters that potentially control differential transcriptional regulation in response to a range of environmental cues. The impact of distinct environmental cues on differential accumulation of ocp homolog transcripts indicates potential functional diversification of this gene family in cyanobacteria. These genes likely enable dynamic cellular protection in response to diverse environmental stress conditions in F. diplosiphon.https://www.frontiersin.org/articles/10.3389/fmicb.2021.819604/fullcyanobacterianon-photochemical quenching (NPQ)orange carotenoid protein (OCP)photosynthesisstress
spellingShingle D. Isabel Petrescu
D. Isabel Petrescu
Preston L. Dilbeck
Beronda L. Montgomery
Beronda L. Montgomery
Beronda L. Montgomery
Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon
Frontiers in Microbiology
cyanobacteria
non-photochemical quenching (NPQ)
orange carotenoid protein (OCP)
photosynthesis
stress
title Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon
title_full Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon
title_fullStr Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon
title_full_unstemmed Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon
title_short Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon
title_sort environmental tuning of homologs of the orange carotenoid protein encoding gene in the cyanobacterium fremyella diplosiphon
topic cyanobacteria
non-photochemical quenching (NPQ)
orange carotenoid protein (OCP)
photosynthesis
stress
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.819604/full
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