Carbon assimilation in upper subtidal macroalgae is determined by an inverse correlation between Rubisco carboxylation efficiency and CO₂ concentrating mechanism effectiveness

Abstract

Summary Seaweeds have a wide ecophysiological and phylogenetic diversity with species expressing different Rubisco forms that frequently coexist with biophysical CO2 concentrating mechanisms (CCMs), an adaptation that overcomes the low CO2 availability and gas diffusion in seawater. Here, we assess the possible coevolution between the Rubisco catalysis and the type and effectiveness of CCMs present in six upper subtidal macroalgal species belonging to three phylogenetic groups of seaweeds. A wide diversity in the Rubisco kinetic traits was found across the analyzed species, although the specificity factor was the only parameter explained by the expressed Rubisco form. Differences in the catalytic trade‐offs were found between Rubisco forms, indicating that ID Rubiscos could be better adapted to the intracellular O2 : CO2 ratio found in marine organisms during steady‐state photosynthesis. The biophysical components of the CCMs also differed among macroalgal species, resulting in different effectiveness to concentrate CO2 around Rubisco active sites. Interestingly, an inverse relationship was found between the effectiveness of CCMs and the in vitro Rubisco carboxylation efficiency, which possibly led to a similar carboxylation potential across the analyzed macroalgal species. Our results demonstrate a coevolution between Rubisco kinetics and CCMs across phylogenetically distant marine macroalgal species sharing the same environment.

Singular adaptations in the carbon assimilation mechanism of the polyextremophile cyanobacterium Chroococcidiopsis thermalis

“…Thus, C. thermalis not only evolved improved Rubisco carboxylation kinetics but also stronger CCMs than other cyanobacterial strains. This response does not follow the inverse relationship between Rubisco carboxylation efficiency and CCM effectiveness previously observed in other photosynthetic groups (Capó-Bauçà et al 2022a , b ) and might indicate that co-evolution between CCMs and Rubisco kinetics in some cyanobacteria is not as constrained as in other phylogenetic groups.…”

The diversity and coevolution of Rubisco and CO2 concentrating mechanisms in marine macrophytes

“…One way to detect these CCMs is using stilbene inhibitors of anion exchange transporters, like 4,4′‐di‐isothiocyanatostilbene‐2,2′‐disulfonate (DIDS) or 4‐acetamido‐4′‐isothiocyanostilbene‐2,2′‐disulfonic acid (SITS), a method first used by Drechsler & Beer (1991) in Ulva latuca . Using this method, several macroalgae species have been identified as DIDS‐sensitive (Drechsler et al ., 1993; Raven & Hurd, 2012; Fernández et al ., 2014; Capó‐Bauçà et al ., 2023). Contrarily, the impact of anion exchange inhibitors on seagrass CCMs has been minimal (Rubio et al ., 2017; Capó‐Bauçà et al ., 2022a).…”

“…Relationship between the effectiveness to concentrate CO 2 around Rubisco ( K c air / K m ) and the in vitro Rubisco carboxylation efficiency at 21% of O 2 ( k cat c / K c air ) of the macrophyte species reported by Capó‐Bauçà et al . (2022a,b, 2023). P ‐value and R 2 were obtained from iterative estimation and linear approximation of nonlinear regression explained in Bates & Watts (1998) (***, P < 0.001).…”

“…Our analysis challenges and expands the previously established paradigm predominantly based on terrestrial vascular plants. The mounting body of evidence up to date (Young et al ., 2016; Flamholz et al ., 2019; Iñiguez et al ., 2019; Davidi et al ., 2020; Goudet et al ., 2020; Bouvier et al ., 2021, 2023; Capó‐Bauçà et al ., 2022a,b, 2023) highlights the necessity for a more extensive and diverse Rubisco research. Such continued efforts are crucial for deepening our understanding of this enzyme's adaptation and evolution across different life forms, which remains an important focus for future work in the field.…”

“…This mechanism can be identified through the inhibition of biophysical CCM components while measuring photosynthetic rates, by using CA inhibitors such as acetazolamide (AZ) or pH buffers that dissipate H + gradients (Beer et al ., 2002; Larkum et al ., 2017). Over the last decades, evidence has been collected supporting the operation of this mechanism in various macroalgal (Koch et al ., 2013; Capó‐Bauçà et al ., 2023) and seagrass species (Hellblom et al ., 2001; Beer et al ., 2002; Uku et al ., 2005; Borum et al ., 2016; Capó‐Bauçà et al ., 2022a,b), indicating that this type of CCM is commonly expressed by marine macrophytes. This mechanism has been proposed to be particularly specialized in seagrasses, possibly due to transfer cell‐like structures in their epidermis (Larkum et al ., 2017).…”