Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component
The marine Synechococcus and Prochlorococcus are the numerically dominant cyanobacteria in the ocean and important in global carbon fixation. They have evolved a CO2-concentrating-mechanism, of which the central component is the carboxysome, a self-assembling proteinaceous organelle. Two types of c...
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MDPI AG
2015-03-01
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| Online Access: | http://www.mdpi.com/2075-1729/5/2/1141 |
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| author | Fei Cai Zhicheng Dou Susan L. Bernstein Ryan Leverenz Eric B. Williams Sabine Heinhorst Jessup Shively Gordon C. Cannon Cheryl A. Kerfeld |
| author_facet | Fei Cai Zhicheng Dou Susan L. Bernstein Ryan Leverenz Eric B. Williams Sabine Heinhorst Jessup Shively Gordon C. Cannon Cheryl A. Kerfeld |
| author_sort | Fei Cai |
| collection | DOAJ |
| description | The marine Synechococcus and Prochlorococcus are the numerically dominant cyanobacteria in the ocean and important in global carbon fixation. They have evolved a CO2-concentrating-mechanism, of which the central component is the carboxysome, a self-assembling proteinaceous organelle. Two types of carboxysome, α and β, encapsulating form IA and form IB d-ribulose-1,5-bisphosphate carboxylase/oxygenase, respectively, differ in gene organization and associated proteins. In contrast to the β-carboxysome, the assembly process of the α-carboxysome is enigmatic. Moreover, an absolutely conserved α-carboxysome protein, CsoS2, is of unknown function and has proven recalcitrant to crystallization. Here, we present studies on the CsoS2 protein in three model organisms and show that CsoS2 is vital for α-carboxysome biogenesis. The primary structure of CsoS2 appears tripartite, composed of an N-terminal, middle (M)-, and C-terminal region. Repetitive motifs can be identified in the N- and M-regions. Multiple lines of evidence suggest CsoS2 is highly flexible, possibly an intrinsically disordered protein. Based on our results from bioinformatic, biophysical, genetic and biochemical approaches, including peptide array scanning for protein-protein interactions, we propose a model for CsoS2 function and its spatial location in the α-carboxysome. Analogies between the pathway for β-carboxysome biogenesis and our model for α-carboxysome assembly are discussed. |
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| last_indexed | 2024-04-11T18:23:09Z |
| publishDate | 2015-03-01 |
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| series | Life |
| spelling | doaj.art-66a803cd44354f8d824ed549dcc1f7032022-12-22T04:09:43ZengMDPI AGLife2075-17292015-03-01521141117110.3390/life5021141life5021141Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical ComponentFei Cai0Zhicheng Dou1Susan L. Bernstein2Ryan Leverenz3Eric B. Williams4Sabine Heinhorst5Jessup Shively6Gordon C. Cannon7Cheryl A. Kerfeld8Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USADepartment of Chemistry and Biochemistry, The University of Southern Mississippi, Hattiesburg, MS 39406-5043, USADepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USAMSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824, USADepartment of Chemistry and Biochemistry, The University of Southern Mississippi, Hattiesburg, MS 39406-5043, USADepartment of Chemistry and Biochemistry, The University of Southern Mississippi, Hattiesburg, MS 39406-5043, USADepartment of Genetics and Biochemistry, Clemson University, Clemson, SC 29634, USADepartment of Chemistry and Biochemistry, The University of Southern Mississippi, Hattiesburg, MS 39406-5043, USADepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USAThe marine Synechococcus and Prochlorococcus are the numerically dominant cyanobacteria in the ocean and important in global carbon fixation. They have evolved a CO2-concentrating-mechanism, of which the central component is the carboxysome, a self-assembling proteinaceous organelle. Two types of carboxysome, α and β, encapsulating form IA and form IB d-ribulose-1,5-bisphosphate carboxylase/oxygenase, respectively, differ in gene organization and associated proteins. In contrast to the β-carboxysome, the assembly process of the α-carboxysome is enigmatic. Moreover, an absolutely conserved α-carboxysome protein, CsoS2, is of unknown function and has proven recalcitrant to crystallization. Here, we present studies on the CsoS2 protein in three model organisms and show that CsoS2 is vital for α-carboxysome biogenesis. The primary structure of CsoS2 appears tripartite, composed of an N-terminal, middle (M)-, and C-terminal region. Repetitive motifs can be identified in the N- and M-regions. Multiple lines of evidence suggest CsoS2 is highly flexible, possibly an intrinsically disordered protein. Based on our results from bioinformatic, biophysical, genetic and biochemical approaches, including peptide array scanning for protein-protein interactions, we propose a model for CsoS2 function and its spatial location in the α-carboxysome. Analogies between the pathway for β-carboxysome biogenesis and our model for α-carboxysome assembly are discussed.http://www.mdpi.com/2075-1729/5/2/1141CO2 concentrating mechanism (CCM)carboxysomeRuBisCOCsoS2assemblyintrinsically disordered proteinpeptide array |
| spellingShingle | Fei Cai Zhicheng Dou Susan L. Bernstein Ryan Leverenz Eric B. Williams Sabine Heinhorst Jessup Shively Gordon C. Cannon Cheryl A. Kerfeld Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component Life CO2 concentrating mechanism (CCM) carboxysome RuBisCO CsoS2 assembly intrinsically disordered protein peptide array |
| title | Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component |
| title_full | Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component |
| title_fullStr | Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component |
| title_full_unstemmed | Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component |
| title_short | Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component |
| title_sort | advances in understanding carboxysome assembly in prochlorococcus and synechococcus implicate csos2 as a critical component |
| topic | CO2 concentrating mechanism (CCM) carboxysome RuBisCO CsoS2 assembly intrinsically disordered protein peptide array |
| url | http://www.mdpi.com/2075-1729/5/2/1141 |
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