Abstract
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 CO2-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 (Km) and turnover rate (kcat) for both CO2 and O2. The pyrenoid-containing T. lutea and P. carterae showed lower Rubisco content and carboxylation properties (KC and kCcat) 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 kCcat-KC relationship and increased CO2/O2 specificity that, when modeled in the context of a C3 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 CO2:O2 microenvironments has probably influenced the divergent evolution of Form 1B and 1D Rubisco kinetics.
Highlights
The CO2-fixing enzyme Rubisco (EC 4.1.1.39) evolved in the Archaean Eon when the atmosphere lacked O2, and CO2 was estimated to be 50-fold higher than current levels (Berner and Canfield, 1989; Berner, 2006; Tabita et al, 2008)
A central objective of this study was to examine the correlations between pyrenoid morphology, evidence of a concentrating mechanism (CCM), and the content and catalysis of Rubisco in microalgae
Phaeodactylum tricornutum was included in this study and, like many members of the lineage, has pyrenoids that are fully immersed within the chloroplast with 1–2 pyrenoid-traversing thylakoids (Borowitzka and Volcani, 1978; Bedoshvili et al, 2009) (Fig. 2A)
Summary
The CO2-fixing enzyme Rubisco (EC 4.1.1.39) evolved in the Archaean Eon when the atmosphere lacked O2, and CO2 was estimated to be 50-fold higher than current levels (Berner and Canfield, 1989; Berner, 2006; Tabita et al, 2008). Recent work showed that the characteristic faster CO2 fixation rates (kCcat) and lower CO2 affinities (i.e. higher Km for CO2; KC) observed in Form 1A and Form 1B Rubisco [e.g. in Chlamydomonas with a pyrenoid-based CO2-concentrating mechanism (CCM)] (Badger et al, 1998; Ghannoum et al, 2005; Sharwood et al, 2016a) are not shared by diatom Form 1D Rubisco (Hanson, 2016; Young et al, 2016; see Fig. 3A) This has led to calls for a more expansive analysis of Rubisco’s natural kinetic diversity so that we can fully understand the correlative interactions between specificity for CO2 as opposed to O2 (SC/O), kCcat, and KC. The one-dimensional, linear correlations previously proposed (Tcherkez et al, 2006; Savir et al, 2010) may vary with photosynthetic taxa (Tcherkez, 2013, 2016; Hanson, 2016; Sharwood, 2017)
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