Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Redox Regulation of a Light-Harvesting Antenna Complex in an Anoxygenic Phototroph

Journal Article · · mBio (Online)
ABSTRACT

The purple nonsulfur bacterium Rhodopseudomonas palustris is a model for understanding how a phototrophic organism adapts to changes in light intensity because it produces different light-harvesting (LH) complexes under high light (LH2) and low light intensities (LH3 and LH4). Outside of this change in the composition of the photosystem, little is understood about how R. palustris senses and responds to low light intensity. On the basis of the results of transcription analysis of 17 R. palustris strains grown in low light, we found that R. palustris strains downregulate many genes involved in iron transport and homeostasis. The only operon upregulated in the majority of R. palustris exposed to low light intensity was pucBAd , which encodes LH4. In previous work, pucBAd expression was shown to be modulated in response to light quality by bacteriophytochromes that are part of a low-light signal transduction system. Here we found that this signal transduction system also includes a redox-sensitive protein, LhfE, and that its redox sensitivity is required for LH4 synthesis in response to low light. Our results suggest that R. palustris upregulates its LH4 system when the cellular redox state is relatively oxidized. Consistent with this, we found that LH4 synthesis was upregulated under high light intensity when R. palustris was grown semiaerobically or under nitrogen-fixing conditions. Thus, changes in the LH4 system in R. palustris are not dependent on light intensity per se but rather on cellular redox changes that occur as a consequence of changes in light intensity.

IMPORTANCE An essential aspect of the physiology of phototrophic bacteria is their ability to adjust the amount and composition of their light-harvesting apparatus in response to changing environmental conditions. The phototrophic purple bacterium R. palustris adapts its photosystem to a range of light intensities by altering the amount and composition of its peripheral LH complexes. Here we found that R. palustris regulates its LH4 complex in response to the cellular redox state rather than in response to light intensity per se . Relatively oxidizing conditions, including low light, semiaerobic growth, and growth under nitrogen-fixing conditions, all stimulated a signal transduction system to activate LH4 expression. By understanding how LH composition is regulated in R. palustris , we will gain insight into how and why a photosynthetic organism senses and adapts its photosystem to multiple environmental cues.

Research Organization:
Univ. of Minnesota, St. Paul, MN (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Chemical Sciences, Geosciences & Biosciences Division
Grant/Contract Number:
SC0020252
OSTI ID:
1575784
Alternate ID(s):
OSTI ID: 1594057
Journal Information:
mBio (Online), Journal Name: mBio (Online) Journal Issue: 6 Vol. 10; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (43)

Changes in carotenoid biosynthesis caused by variations of growth conditions in cultures of Rhodopseudomonas acidophila strain 7050 journal June 1983
Differentiation of the intracytoplasmic membrane of Rhodopseudomonas palustris induced by variations of oxygen partial pressure or light intensity journal January 1977
Bacteriophytochrome-Dependent Regulation of Light-Harvesting Complexes in Rhodopseudomonas palustris Anaerobic Cultures journal April 2010
A bacteriophytochrome regulates the synthesis of LH4 complexesin Rhodopseudomonas palustris journal August 2005
Bacteriophytochromes in anoxygenic photosynthetic bacteria journal July 2008
Evolution of low-light adapted peripheral light-harvesting complexes in strains of Rhodopseudomonas palustris journal December 2012
Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris journal October 1991
The 7.5-Å Electron Density and Spectroscopic Properties of a NovelLow-Light B800 LH2 from Rhodopseudomonas palustris journal February 2002
Single-Molecule Spectroscopy Reveals that Individual Low-Light LH2 Complexes from Rhodopseudomonas palustris 2.1.6. Have a Heterogeneous Polypeptide Composition journal September 2009
Low Light Adaptation: Energy Transfer Processes in Different Types of Light Harvesting Complexes from Rhodopseudomonas palustris journal December 2009
Acclimation strategy of Rhodopseudomonas palustris to high light irradiance journal April 2017
The structural basis of light-harvesting in purple bacteria journal October 2003
Interaction between the Bacterial Iron Response Regulator and Ferrochelatase Mediates Genetic Control of Heme Biosynthesis journal January 2002
Rhodopseudomonas palustris CGA009 Has Two Functional ppsR Genes, Each of Which Encodes a Repressor of Photosynthesis Gene Expression journal December 2006
Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris journal December 2003
Evolution of a bacteriophytochrome from light to redox sensor journal June 2007
Adaptation of Rhodopseudomonas acidophila strain 7050 to growth at different light intensities: what are the benefits to changing the type of LH2? journal January 2018
The light intensity under which cells are grown controls the type of peripheral light-harvesting complexes that are assembled in a purple photosynthetic bacterium journal October 2011
Multiple genome sequences reveal adaptations of a phototrophic bacterium to sediment microenvironments journal November 2008
Tracking energy transfer between light harvesting complex 2 and 1 in photosynthetic membranes grown under high and low illumination journal January 2012
Apo-bacteriophytochromes modulate bacterial photosynthesis in response to low light journal December 2013
Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein journal November 1999
Heme-responsive DNA Binding by the Global Iron Regulator Irr from Rhizobium leguminosarum journal March 2010
PpsR, a Regulator of Heme and Bacteriochlorophyll Biosynthesis, Is a Heme-sensing Protein journal February 2012
RegB Kinase Activity Is Repressed by Oxidative Formation of Cysteine Sulfenic Acid journal January 2013
A New Type of Bacteriophytochrome Acts in Tandem with a Classical Bacteriophytochrome to Control the Antennae Synthesis in Rhodopseudomonas palustris journal July 2005
Identification of a Ubiquinone-binding Site That Affects Autophosphorylation of the Sensor Kinase RegB journal January 2006
Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria journal January 2012
Growth, Pigmentation, and Expression of the puf and puc Operons in a Light-Responding-Repressor (SPB)-Disrupted Rhodobacter sphaeroides journal April 1998
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes journal September 2003
Structure of the response regulator RPA3017 involved in red-light signaling in Rhodopseudomonas palustris journal September 2015
Activity of the tetrapyrrole regulator CrtJ is controlled by oxidation of a redox active cysteine located in the DNA binding domain: A redox active Cys controls CrtJ DNA binding activity journal July 2012
Identification of a p -Coumarate Degradation Regulon in Rhodopseudomonas palustris by Xpression, an Integrated Tool for Prokaryotic RNA-Seq Data Processing journal July 2012
Redirection of Metabolism for Biological Hydrogen Production journal January 2007
The PpaA/AerR Regulators of Photosynthesis Gene Expression from Anoxygenic Phototrophic Proteobacteria Contain Heme-Binding SCHIC Domains journal July 2010
Hierarchical Regulation of Photosynthesis Gene Expression by the Oxygen-Responsive PrrBA and AppA-PpsR Systems of Rhodobacter sphaeroides journal October 2008
BadR, a New MarR Family Member, Regulates Anaerobic Benzoate Degradation by Rhodopseudomonas palustris in Concert with AadR, an Fnr Family Member journal April 1999
The Iron Control Element, Acting in Positive and Negative Control of Iron-Regulated Bradyrhizobium japonicum Genes, Is a Target for the Irr Protein journal December 2005
Characterization of a light-responding trans-activator responsible for differentially controlling reaction center and light-harvesting-I gene expression in Rhodobacter capsulatus. journal November 1994
RegB Kinase Activity Is Controlled in Part by Monitoring the Ratio of Oxidized to Reduced Ubiquinones in the Ubiquinone Pool journal December 2010
Clades of Photosynthetic Bacteria Belonging to the Genus Rhodopseudomonas Show Marked Diversity in Light-Harvesting Antenna Complex Gene Composition and Expression journal December 2015
Differential expression analysis for sequence count data journal October 2010
Differing isoforms of the cobalamin binding photoreceptor AerR oppositely regulate photosystem expression journal October 2018