Prochlorococcus carbon dioxide-concentrating mechanism: evidence of carboxysome-associated heterogeneity

• Published in: Photosynthesis research Vol. 123; no. 1; pp. 45 - 60
• Main Authors: Ting, Claire S, Dusenbury, Katharine H, Pryzant, Reid A, Higgins, Kathleen W, Pang, Catherine J, Black, Christie E, Beauchamp, Ellen M
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer-Verlag 01.01.2015; Springer Netherlands; Springer; Springer Nature B.V
• Subjects: Amino Acid Sequence; Analysis; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; bicarbonates; Biochemistry; Biomedical and Life Sciences; Biopolymers; carbon; Carbon Cycle; Carbon dioxide; Carbon Dioxide - metabolism; carbon sinks; carbonate dehydratase; Carbonates; cell growth; cellular microenvironment; Chlorophyll; Chromosomes, Bacterial; Cyanobacteria; energy; evolution; gene expression regulation; Gene Expression Regulation, Bacterial - physiology; genes; Genetic diversity; Genome, Bacterial; Genomics; Life Sciences; Molecular Sequence Data; nucleotide sequences; Photosynthesis; Plant Genetics and Genomics; Plant Physiology; Plant Sciences; polypeptides; Prochlorococcus; Prochlorococcus - genetics; Prochlorococcus - metabolism; Regular Paper; ribulose-bisphosphate carboxylase; Synechococcus; Chlorophyll; Global comparative genomics; Microcompartment; Carbonic anhydrase; Oxychlorobacteria; containing cyanobacteria; Genomic diversity
• ISSN: 0166-8595; 1573-5079
• DOI: 10.1007/s11120-014-0038-0

The ability of Prochlorococcus to numerically dominate open ocean regions and contribute significantly to global carbon cycles is dependent in large part on its effectiveness in transforming light energy into compounds used in cell growth, maintenance, and division. Integral to these processes is the carbon dioxide-concentrating mechanism (CCM), which enhances photosynthetic CO₂fixation. The CCM involves both active uptake systems that permit intracellular accumulation of inorganic carbon as the pool of bicarbonate and the system of HCO₃⁻conversion into CO₂. The latter is located in the carboxysome, a microcompartment designed to promote the carboxylase activity of Rubisco. This study presents a comparative analysis of several facets of the Prochlorococcus CCM. Our analyses indicate that a core set of CCM components is shared, and their genomic organization is relatively well conserved. Moreover, certain elements, including carboxysome shell polypeptides CsoS1 and CsoS4A, exhibit striking conservation. Unexpectedly, our analyses reveal that the carbonic anhydrase (CsoSCA) and CsoS2 shell polypeptide have diversified within the lineage. Differences in csoSCA and csoS2 are consistent with a model of unequal rates of evolution rather than relaxed selection. The csoS2 and csoSCA genes form a cluster in Prochlorococcus genomes, and we identified two conserved motifs directly upstream of this cluster that differ from the motif in marine Synechococcus and could be involved in regulation of gene expression. Although several elements of the CCM remain well conserved in the Prochlorococcus lineage, the evolution of differences in specific carboxysome features could in part reflect optimization of carboxysome-associated processes in dissimilar cellular environments.