The role of Rubisco kinetics and pyrenoid morphology in shaping the CCM of haptophyte microalgae

The haptophyte algae are a cosmopolitan group of primary producers that contribute significantly to the marine carbon cycle and play a major role in paleo-climate studies. Despite their global importance, little is known about carbon assimilation in haptophytes, in particular the kinetics of their Form 1D CO(2)-fixing enzyme, Rubisco. Here we examine Rubisco properties of three haptophytes with a range of pyrenoid morphologies (Pleurochrysis carterae, Tisochrysis lutea, and Pavlova lutheri) and the diatom Phaeodactylum tricornutum that exhibit contrasting sensitivities to the trade-offs between substrate affinity (K(m)) and turnover rate (k(cat)) for both CO(2) and O(2). The pyrenoid-containing T. lutea and P. carterae showed lower Rubisco content and carboxylation properties (K(C) and k(C)(cat)) comparable with those of Form 1D-containing non-green algae. In contrast, the pyrenoid-lacking P. lutheri produced Rubisco in 3-fold higher amounts, and displayed a Form 1B Rubisco k(C)(cat)–K(C) relationship and increased CO(2)/O(2) specificity that, when modeled in the context of a C(3) leaf, supported equivalent rates of photosynthesis to higher plant Rubisco. Correlation between the differing Rubisco properties and the occurrence and localization of pyrenoids with differing intracellular CO(2):O(2) microenvironments has probably influenced the divergent evolution of Form 1B and 1D Rubisco kinetics.