Microalgal carbon-dioxide-concentrating mechanisms: Chlamydomonas inorganic carbon transporters.

Aquatic photosynthetic micro-organisms have adapted to the variable and often-limiting availability of CO(2), and inorganic carbon (Ci) in general, by development of inducible CO(2)-concentrating mechanisms (CCMs) that allow them to optimize carbon acquisition. Both microalgal and cyanobacterial CCMs function to facilitate CO(2) assimilation when Ci is limiting via active Ci uptake systems to increase internal Ci accumulation and carbonic anhydrase activity to provide elevated internal CO(2) concentrations through the dehydration of accumulated bicarbonate. These CCMs have been studied over several decades, and details of the cyanobacterial CCM function have emerged over recent years. However, significant advances in understanding of the microalgal CCM have been more recent. With the aid of mutational approaches and the availability of multiple microalgal genome sequences, an integrated picture of the functional components of the microalgal CCMs is emerging, together with the molecular details regarding the function and regulation of the CCM. This review will focus on the recent advances in identifying and characterizing the Ci transport components of the microalgal CCM, especially in the model organism Chlamydomonas reinhardtii Dangeard.

[1]  J. Moroney,et al.  Identification of a New Chloroplast Carbonic Anhydrase in Chlamydomonas reinhardtii1 , 2004, Plant Physiology.

[2]  J. Moroney,et al.  Partial characterization of a new isoenzyme of carbonic anhydrase isolated from Chlamydomonas reinhardtii. , 1991, The Journal of biological chemistry.

[3]  M. Badger,et al.  Journal of Experimental Botany Advance Access published October 10, 2005 Journal of Experimental Botany, Page 1 of 17 Phenotypic Plasticity and the Changing Environment Special Issue , 2005 .

[4]  J. Rochaix,et al.  The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas , 1998, Advances in Photosynthesis and Respiration.

[5]  D. Sültemeyer,et al.  Uptake of CO2 and bicarbonate by intact cells and chloroplasts of Tetraedron minimum and Chlamydomonas noctigama , 2002, Planta.

[6]  M. Spalding,et al.  An inorganic carbon transport system responsible for acclimation specific to air levels of CO2 in Chlamydomonas reinhardtii. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Spalding,et al.  Adaptation of Chlamydomonas reinhardtii High-CO(2)-Requiring Mutants to Limiting CO(2). , 1989, Plant physiology.

[8]  K. Ohyama,et al.  cemA homologue essential to CO2 transport in the cyanobacterium Synechocystis PCC6803. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  A. Grossman,et al.  Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. , 2002, The Plant journal : for cell and molecular biology.

[10]  J. Karlsson,et al.  Effect of vanadate on photosynthesis and the ATP/ADP ratio in low-CO2-adapted Chlamydomonas reinhardtii cells , 1993, Planta.

[11]  J. Moroney,et al.  Isolation of cDNA clones of genes induced upon transfer of Chlamydomonas reinhardtii cells to low CO2 , 1996, Plant Molecular Biology.

[12]  J. Raven,et al.  CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. , 2005, Annual review of plant biology.

[13]  M. Saier,et al.  Expansion of the mitochondrial carrier family. , 1993, Research in microbiology.

[14]  J. Moroney,et al.  The carbonic anhydrase gene families of Chlamydomonas reinhardtii , 2005 .

[15]  H. Fock,et al.  Uptake of HCO 3 2 and CO 2 in Cells and Chloroplasts from the Microalgae Chlamydomonas reinhardtii and Dunaliella tertiolecta 1 , 1998 .

[16]  M. Badger,et al.  Carbonic anhydrase activity and inorganic carbon fluxes in low‐ and high‐C1 cells of Chlamydomonas reinhardtü and Scenedesmus obliquus , 1994 .

[17]  W. Inwood,et al.  Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels. , 2006, Transfusion clinique et biologique : journal de la Societe francaise de transfusion sanguine.

[18]  M. Spalding,et al.  Periplasmic carbonic anhydrase structural gene (Cah1) mutant in chlamydomonas reinhardtii , 1999, Plant physiology.

[19]  E. Fernández,et al.  Differential regulation of the Chlamydomonas Nar1 gene family by carbon and nitrogen. , 2006, Protist.

[20]  G. Schmetterer,et al.  Photosynthetic Electron Transport Involved in PxcA-Dependent Proton Extrusion in Synechocystis sp. Strain PCC6803: Effect of pxcA Inactivation on CO2, HCO3−, and NO3−Uptake , 1998, Journal of bacteriology.

[21]  Martin H. Spalding,et al.  Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states , 2005 .

[22]  G. Espie,et al.  Active CO2 Transport by the Green Alga Chlamydomonas reinhardtii , 1989 .

[23]  M. Badger,et al.  CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. , 2003, Journal of experimental botany.

[24]  S. Lemaire,et al.  The Chlamydomonas reinhardtii proteins Ccp1 and Ccp2 are required for long-term growth, but are not necessary for efficient photosynthesis, in a low-CO2 environment , 2004, Plant Molecular Biology.

[25]  D. Weeks,et al.  Intracellular Carbonic Anhydrase Is Essential to Photosynthesis in Chlamydomonas reinhardtii at Atmospheric Levels of CO2 (Demonstration via Genomic Complementation of the High-CO2-Requiring Mutant ca-1) , 1997, Plant physiology.

[26]  J. Karlsson,et al.  Discovery of an algal mitochondrial carbonic anhydrase: molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[27]  D. Weeks,et al.  The Cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas reinhardtii , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. Spalding,et al.  CO2 Acquisition, Concentration and Fixation in Cyanobacteria and Algae , 2000 .

[29]  T. Ogawa,et al.  Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E. H. Harris,et al.  CHLAMYDOMONAS AS A MODEL ORGANISM. , 2003, Annual review of plant physiology and plant molecular biology.

[31]  M. Badger,et al.  The Chlamydomonas reinhardtii cia3 Mutant Lacking a Thylakoid Lumen-Localized Carbonic Anhydrase Is Limited by CO2 Supply to Rubisco and Not Photosystem II Function in Vivo , 2003, Plant Physiology.

[32]  M. Kitayama,et al.  Evidence for Inorganic Carbon Transport by Intact Chloroplasts of Chlamydomonas reinhardtii. , 1987, Plant physiology.

[33]  Yasukazu Nakamura,et al.  Expression Profiling-Based Identification of CO2-Responsive Genes Regulated by CCM1 Controlling a Carbon-Concentrating Mechanism in Chlamydomonas reinhardtii1 , 2004, Plant Physiology.

[34]  H. Fukuzawa,et al.  cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: regulation by environmental CO2 concentration. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Spalding,et al.  Insertional mutants of Chlamydomonas reinhardtii that require elevated CO(2) for survival. , 2001, Plant physiology.

[36]  W. Inwood,et al.  Lack of the Rhesus protein Rh1 impairs growth of the green alga Chlamydomonas reinhardtii at high CO2. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Badger,et al.  Internal Inorganic Carbon Pool of Chlamydomonas reinhardtii: EVIDENCE FOR A CARBON DIOXIDE-CONCENTRATING MECHANISM. , 1980, Plant Physiology.

[38]  C. Huang,et al.  Rh proteins vs Amt proteins: an organismal and phylogenetic perspective on CO2 and NH3 gas channels. , 2006, Transfusion clinique et biologique : journal de la Societe francaise de transfusion sanguine.

[39]  T. Sharkey,et al.  Photosynthesis : physiology and metabolism , 2000 .

[40]  J. Rexach,et al.  The plastidic nitrite transporter NAR1;1 improves nitrate use efficiency for growth in Chlamydomonas , 2004 .

[41]  J. Raven,et al.  An Anaplerotic Role for Mitochondrial Carbonic Anhydrase in Chlamydomonas reinhardtii1 , 2003, Plant Physiology.

[42]  M. Badger,et al.  Measurement of CO2 and HCO3− fluxes in cyanobacteria and microalgae during steady‐state photosynthesis , 1994 .

[43]  J. Rexach,et al.  The Chlamydomonas reinhardtii Nar1 Gene Encodes a Chloroplast Membrane Protein Involved in Nitrite Transport , 2000, Plant Cell.

[44]  H. Fukuzawa,et al.  Genes Essential to Sodium-dependent Bicarbonate Transport in Cyanobacteria , 2002, The Journal of Biological Chemistry.

[45]  A. Goyal,et al.  Uptake of inorganic carbon by isolated chloroplasts from air-adapted dunaliella. , 1989, Plant Physiology.

[46]  J. Moroney,et al.  Cloning and Overexpression of Two cDNAs Encoding the Low-CO2-lnducible Chloroplast Envelope Protein LIP-36 from Chlamydomonas reinhardtii , 1997, Plant Physiology.

[47]  D. Baurain,et al.  A Comparative Inventory of Metal Transporters in the Green Alga Chlamydomonas reinhardtii and the Red Alga Cyanidioschizon merolae1[w] , 2005, Plant Physiology.

[48]  H. Fukuzawa,et al.  Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: Genes involved and their phylogenetic relationship with homologous genes in other organisms , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. A. Rea Plant ATP-binding cassette transporters. , 2007, Annual review of plant biology.

[50]  M. Spalding,et al.  Acclimation of Chlamydomonas to changing carbon availability. , 2002, Functional plant biology : FPB.

[51]  A. Goyal,et al.  Two Systems for Concentrating CO(2) and Bicarbonate during Photosynthesis by Scenedesmus. , 1990, Plant physiology.

[52]  J. Vanderleyden,et al.  Identification of an ATP-binding Cassette Transporter for Export of the O-antigen across the Inner Membrane inRhizobium etli Based on the Genetic, Functional, and Structural Analysis of an lps Mutant Deficient in O-antigen* , 2001, The Journal of Biological Chemistry.

[53]  H. Fukuzawa,et al.  Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[54]  M. Spalding,et al.  Carbonic Anhydrase-Deficient Mutant of Chlamydomonas reinhardii Requires Elevated Carbon Dioxide Concentration for Photoautotrophic Growth. , 1983, Plant physiology.

[55]  M. Spalding,et al.  The Low CO2-Inducible 36-Kilodalton Protein Is Localized to the Chloroplast Envelope of Chlamydomonas reinhardtii , 1993, Plant physiology.

[56]  K. Ohyama,et al.  Ccm1, a regulatory gene controlling the induction of a carbon-concentrating mechanism in Chlamydomonas reinhardtii by sensing CO2 availability , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Kaplan,et al.  The Location of the Transporting System for Inorganic Carbon and the Nature of the Form Translocated in Chlamydomonas reinhardtii , 1984 .

[58]  J. Moroney,et al.  Evidence That an Internal Carbonic Anhydrase Is Present in 5% CO(2)-Grown and Air-Grown Chlamydomonas. , 1987, Plant physiology.

[59]  T. Ogawa,et al.  Absence of light-induced proton extrusion in a cotA-less mutant of Synechocystis sp. strain PCC6803 , 1996, Journal of bacteriology.

[60]  Simon Prochnik,et al.  Novel metabolism in Chlamydomonas through the lens of genomics. , 2007, Current opinion in plant biology.

[61]  M. Badger,et al.  CO 2 concentrating mechanisms in cyanobacteria : molecular components , their diversity and evolution , 2022 .

[62]  J. Moroney,et al.  Complementation analysis of the inorganic carbon concentrating mechanism of Chlamydomonas reinhardtii , 1986, Molecular and General Genetics MGG.

[63]  S. Maeda,et al.  Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942. , 2002, Functional plant biology : FPB.

[64]  K. Kreuzberg,et al.  Photosynthesis and apparent affinity for dissolved inorganic carbon by cells and chloroplasts of Chlamydomonas reinhardtii grown at high and low CO2 concentrations , 1988, Planta.

[65]  S. Maeda,et al.  Novel gene products associated with NdhD3/D4‐containing NDH‐1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942 , 2002, Molecular microbiology.

[66]  M. Spalding,et al.  Reduced Inorganic Carbon Transport in a CO(2)-Requiring Mutant of Chlamydomonas reinhardii. , 1983, Plant physiology.

[67]  S. Howitt,et al.  Identification of a SulP-type bicarbonate transporter in marine cyanobacteria , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[68]  J. Moroney,et al.  A novel α‐type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2 , 1998 .

[69]  J. Moroney,et al.  The intracellular localization of ribulose-1,5-bisphosphate Carboxylase/Oxygenase in chlamydomonas reinhardtii , 1998, Plant physiology.

[70]  M. Spalding Acquisition. Acclimation to Changing Carbon Availability , 1998 .

[71]  K. Niyogi,et al.  Rhesus expression in a green alga is regulated by CO2 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[72]  J. Moroney,et al.  The role of the chloroplast in inorganic carbon acquisition by Chlamydomonas reinhardtii , 1991 .

[73]  F. Palmieri Mitochondrial carrier proteins , 1994, FEBS letters.

[74]  J. Rexach,et al.  Nitrite transport to the chloroplast in Chlamydomonas reinhardtii: molecular evidence for a regulated process. , 2002, Journal of experimental botany.

[75]  S. Sjöberg,et al.  Induction of Inorganic Carbon Accumulation in the Unicellular Green Algae Scenedesmus obliquus and Chlamydomonas reinhardtii. , 1988, Plant physiology.

[76]  D. Hewett‐Emmett,et al.  Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. , 1996, Molecular phylogenetics and evolution.

[77]  A. Kaplan,et al.  CO2 CONCENTRATING MECHANISMS IN PHOTOSYNTHETIC MICROORGANISMS. , 1999, Annual review of plant physiology and plant molecular biology.

[78]  J. Rochaix,et al.  Disruption of the plastid ycf10 open reading frame affects uptake of inorganic carbon in the chloroplast of Chlamydomonas , 1997, The EMBO journal.

[79]  H. Fukuzawa,et al.  The Novel Myb Transcription Factor LCR1 Regulates the CO2-Responsive Gene Cah1, Encoding a Periplasmic Carbonic Anhydrase in Chlamydomonas reinhardtii , 2004, The Plant Cell Online.