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

Abstract

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 CO2 fixation. 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.

The impact of elevated CO2 on Prochlorococcus and microbial interactions with ‘helper’ bacterium Alteromonas

“…There was no significant change in expression of the bicarbonate transporter genes ( Supplementary Table 2) in agreement with a previous study on MED4 (Hopkinson et al, 2014). Our data suggest that carboxysome and bicarbonate transporter genes are regulated by separate mechanisms, a conclusion supported by the existence of different conserved sequence motifs for carboxysome subunits and bicarbonate transporters in Prochlorococcus strains (Ting et al, 2015). The lack of a significant shift in expression of energy-consuming bicarbonate transporter genes may indicate that there would not be a significant energetic savings for Prochlorococcus under elevated CO 2 .…”

“…One of the significantly differentially expressed carboxysome subunit genes, csoSCA, also functions as a carbonic anhydrase (So et al, 2004;Ting et al, 2015). The observed decreased expression of csoSCA supports the hypothesis that under elevated CO 2 , phytoplankton downregulates CCM genes because of increased diffusive supply of CO 2 , or pH-induced transcriptional regulation.…”

Advances in Understanding Carboxysome Assembly in Prochlorococcus and Synechococcus Implicate CsoS2 as a Critical Component

“…Although CsoS2 has the least conserved primary structure among all α-carboxysome proteins [ 27 , 28 ], some unusual sequence features are shared among Hnea CsoS2 and its counterparts in Prochlorococcus strains. First, the three CsoS2 proteins from Hnea , MED4 and MIT9313 have unusually high pI values ( Table 1 ).…”

Measuring the in situ carbon isotopic composition of distinct marine plankton populations sorted by flow cytometry

“…Prochlorococcus is not always found in the waters off the SIO Pier (Worden et al ) and was absent during our other sampling time points, so we do not know if this more 13 C‐enriched value is typical for this species group in situ. Differences have been identified in carboxysome‐associated components of the carbon dioxide‐concentrating mechanisms between Prochlorococcus and Synechococcus (Ting et al ), which could be responsible for the different δ 13 C values for cyanobacterial groups sorted from the same seawater sample. Alternatively, the Prochlorococcus population sampled could have been at a more advanced growth stage (i.e., stationary; Brutemark et al ), or assimilating carbon from organic substrates such as amino acids (Zubkov et al ; Michelou et al ).…”