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Title: Linking the Dynamic Response of the Carbon Dioxide-Concentrating Mechanism to Carbon Assimilation Behavior in Fremyella diplosiphon

Journal Article · · mBio (Online)
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ABSTRACT Cyanobacteria use a carbon dioxide (CO 2 )-concentrating mechanism (CCM) that enhances their carbon fixation efficiency and is regulated by many environmental factors that impact photosynthesis, including carbon availability, light levels, and nutrient access. Efforts to connect the regulation of the CCM by these factors to functional effects on carbon assimilation rates have been complicated by the aqueous nature of cyanobacteria. Here, we describe the use of cyanobacteria in a semiwet state on glass fiber filtration discs—cyanobacterial discs—to establish dynamic carbon assimilation behavior using gas exchange analysis. In combination with quantitative PCR (qPCR) and transmission electron microscopy (TEM) analyses, we linked the regulation of CCM components to corresponding carbon assimilation behavior in the freshwater, filamentous cyanobacterium Fremyella diplosiphon . Inorganic carbon (C i ) levels, light quantity, and light quality have all been shown to influence carbon assimilation behavior in F. diplosiphon . Our results suggest a biphasic model of cyanobacterial carbon fixation. While behavior at low levels of CO 2 is driven mainly by the C i uptake ability of the cyanobacterium, at higher CO 2 levels, carbon assimilation behavior is multifaceted and depends on C i availability, carboxysome morphology, linear electron flow, and cell shape. Carbon response curves (CRCs) generated via gas exchange analysis enable rapid examination of CO 2 assimilation behavior in cyanobacteria and can be used for cells grown under distinct conditions to provide insight into how CO 2 assimilation correlates with the regulation of critical cellular functions, such as the environmental control of the CCM and downstream photosynthetic capacity. IMPORTANCE Environmental regulation of photosynthesis in cyanobacteria enhances organismal fitness, light capture, and associated carbon fixation under dynamic conditions. Concentration of carbon dioxide (CO 2 ) near the carbon-fixing enzyme RubisCO occurs via the CO 2 -concentrating mechanism (CCM). The CCM is also tuned in response to carbon availability, light quality or levels, or nutrient access—cues that also impact photosynthesis. We adapted dynamic gas exchange methods generally used with plants to investigate environmental regulation of the CCM and carbon fixation capacity using glass fiber-filtered cells of the cyanobacterium Fremyella diplosiphon . We describe a breakthrough in measuring real-time carbon uptake and associated assimilation capacity for cells grown in distinct conditions (i.e., light quality, light quantity, or carbon status). These measurements demonstrate that the CCM modulates carbon uptake and assimilation under low-C i conditions and that light-dependent regulation of pigmentation, cell shape, and downstream stages of carbon fixation are critical for tuning carbon uptake and assimilation.

Research Organization:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
Grant/Contract Number:
FG02-91ER20021
OSTI ID:
1630757
Alternate ID(s):
OSTI ID: 1735826
Journal Information:
mBio (Online), Journal Name: mBio (Online) Vol. 11 Journal Issue: 3; ISSN 2150-7511
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

References (61)

Photoregulation of Cellular Morphology during Complementary Chromatic Adaptation Requires Sensor-Kinase-Class Protein RcaE in Fremyella diplosiphon journal April 2008
Light Modulates the Biosynthesis and Organization of Cyanobacterial Carbon Fixation Machinery through Photosynthetic Electron Flow journal March 2016
Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: Genes involved and their phylogenetic relationship with homologous genes in other organisms journal September 2001
Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of Rubisco and the mode of inorganic carbon transport in cells of the cyanobacterium Synechococcus UTEX 625 journal January 1993
Cyanobacterial carboxysomes contain an unique rubisco‐activase‐like protein journal October 2019
Expression and Functional Roles of the Two Distinct NDH-1 Complexes and the Carbon Acquisition Complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp PCC 6803 journal November 2004
Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error journal September 2003
A Multiprotein Bicarbonate Dehydration Complex Essential to Carboxysome Function in Cyanobacteria journal November 2007
RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness: Characterization of the RcaE photoreceptor journal January 2004
Isolation and Characterization of High CO 2 -Requiring-Mutants of the Cyanobacterium Synechococcus PCC7942 : Two Phenotypes that Accumulate Inorganic Carbon but Are Apparently Unable to Generate CO journal October 1989
DNA Microarray Analysis of Cyanobacterial Gene Expression during Acclimation to High Light journal April 2001
Involvement of a CbbR Homolog in Low CO2-Induced Activation of the Bicarbonate Transporter Operon in Cyanobacteria journal March 2001
Stepwise Photoinhibition of Photosystem II: Studies with Synechocystis Species PCC 6803 Mutants with a Modified D-E Loop of the Reaction Center Polypeptide D1 journal June 1998
Structural Determinants of the Outer Shell of β-Carboxysomes in Synechococcus elongatus PCC 7942: Roles for CcmK2, K3-K4, CcmO, and CcmL journal August 2012
Complementary Chromatic Adaptation in a Filamentous Blue-Green alga journal August 1973
Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors journal September 1996
Morphogenes bolA and mreB mediate the photoregulation of cellular morphology during complementary chromatic acclimation in F remyella diplosiphon : Photoregulation of morphogenes mediates cell shape journal May 2014
The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments journal February 2009
Heterohexamers Formed by CcmK3 and CcmK4 Increase the Complexity of Beta Carboxysome Shells journal November 2018
Alterations in Global Patterns of Gene Expression in Synechocystis sp. PCC 6803 in Response to Inorganic Carbon Limitation and the Inactivation of ndhR , a LysR Family Regulator journal November 2003
Random Insertional Mutagenesis Used in the Generation of Mutants of the Marine Cyanobacterium Synechococcus sp. Strain PCC7002 With an Impaired CO2 Concentrating Mechanism journal January 1997
Regulation of CO2 Concentrating Mechanism in Cyanobacteria journal January 2015
Emerging Perspectives on the Mechanisms, Regulation, and Distribution of Light Color Acclimation in Cyanobacteria journal January 2012
Measurement of CO2 and HCO3- fluxes in cyanobacteria and microalgae during steady-state photosynthesis journal March 1994
Atomic-Level Models of the Bacterial Carboxysome Shell journal February 2008
Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942 journal November 1999
Photosynthesis and fluorescence responses of C4 plant Andropogon gerardii acclimated to temperature and carbon dioxide journal September 2008
Detection of oxygen-evolving Photosystem II centers inactive in plastoquinone reduction journal December 1986
Elucidating Essential Role of Conserved Carboxysomal Protein CcmN Reveals Common Feature of Bacterial Microcompartment Assembly journal March 2012
A modular system for the measurement of CO 2 and O 2 gas flux and photosynthetic electron transport in microalgae : Algal photosynthetic efficiency system journal December 2012
Interrelated modules in cyanobacterial photosynthesis: the carbon-concentrating mechanism, photorespiration, and light perception journal April 2016
Biogenesis of a Bacterial Organelle: The Carboxysome Assembly Pathway journal November 2013
Mechanisms and fitness implications of photomorphogenesis during chromatic acclimation in cyanobacteria journal May 2016
Metabolic and Transcriptomic Phenotyping of Inorganic Carbon Acclimation in the Cyanobacterium Synechococcus elongatus PCC 7942 journal January 2011
Regulation of the carbon-concentrating mechanism in the cyanobacterium Synechocystis sp. PCC6803 in response to changing light intensity and inorganic carbon availability journal August 2013
Genes Essential to Sodium-dependent Bicarbonate Transport in Cyanobacteria: FUNCTION AND PHYLOGENETIC ANALYSIS journal March 2002
ISOLATION OF ccmKLMN GENES FROM THE MARINE CYANOBACTERIUM, SYNECHOCOCCUS SP. PCC7002 (CYANOPHYCEAE), AND EVIDENCE THAT CcmM IS ESSENTIAL FOR CARBOXYSOME ASSEMBLY journal December 2000
Inorganic Carbon Limitation and Light Control the Expression of Transcripts Related to the CO 2 -Concentrating Mechanism in the Cyanobacterium Synechocystis sp. Strain PCC6803 journal April 2003
Systems analysis of the CO2 concentrating mechanism in cyanobacteria journal April 2014
Construction of Shuttle Plasmids Which Can Be Efficiently Mobilized from Escherichia coli into the Chromatically Adapting Cyanobacterium, Fremyella diplosiphon journal September 1993
Analysis of a genomic DNA region from the cyanobacterium Synechococcus sp. strain PCC7942 involved in carboxysome assembly and function. journal May 1993
Rubisco condensate formation by CcmM in β-carboxysome biogenesis journal January 2019
Identification of a SulP-type bicarbonate transporter in marine cyanobacteria journal December 2004
The small RbcS-like domains of the β-carboxysome structural protein CcmM bind RubisCO at a site distinct from that binding the RbcS subunit journal December 2018
Carboxysomes: metabolic modules for CO2 fixation journal August 2017
Rubisco regulation: a role for inhibitors journal June 2007
Temporal responses of wild-type pigmentation and RcaE-deficient strains of Fremyella diplosiphon during light transitions journal September 2011
The Structure of CcmP, a Tandem Bacterial Microcompartment Domain Protein from the β-Carboxysome, Forms a Subcompartment Within a Microcompartment journal April 2013
Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light: Estimates from gas-exchange measurements on spinach journal January 1985
Two new high-resolution crystal structures of carboxysome pentamer proteins reveal high structural conservation of CcmL orthologs among distantly related cyanobacterial species journal August 2013
Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942: Mechanism of CO2 uptake in cyanobacteria journal January 2002
RcaE-Dependent Regulation of Carboxysome Structural Proteins Has a Central Role in Environmental Determination of Carboxysome Morphology and Abundance in Fremyella diplosiphon journal January 2018
Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix journal May 1996
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species journal June 1980
CO 2 Fixation Kinetics of Halothiobacillus neapolitanus Mutant Carboxysomes Lacking Carbonic Anhydrase Suggest the Shell Acts as a Diffusional Barrier for CO 2 journal February 2008
β-Carboxysome bioinformatics: identification and evolution of new bacterial microcompartment protein gene classes and core locus constraints journal April 2017
Single-Organelle Quantification Reveals Stoichiometric and Structural Variability of Carboxysomes Dependent on the Environment journal May 2019
Membrane-Inlet Mass Spectrometry Enables a Quantitative Understanding of Inorganic Carbon Uptake Flux and Carbon Concentrating Mechanisms in Metabolically Engineered Cyanobacteria journal June 2019
Long-Term Response toward Inorganic Carbon Limitation in Wild Type and Glycolate Turnover Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 6803 journal June 2007
Protein Structures Forming the Shell of Primitive Bacterial Organelles journal August 2005
Photosynthesis and Inorganic Carbon Usage by the Marine Cyanobacterium, Synechococcus sp journal August 1982

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Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Carbon dioxide assimilation
carbon dioxide concentration mechanism
carbon dioxide fixation
carboxysome
cyanobacteria
gas exchange