Rubisco and carbon-concentrating mechanism co-evolution across chlorophyte and streptophyte green algae.

Myriam M M Goudet,Douglas J Orr,Karin H Müller,Michael Melkonian,Howard Griffiths,Moritz T Meyer,Elizabete Carmo‐Silva

doi:10.1111/nph.16577

Abstract

Green algae expressing a carbon-concentrating mechanism (CCM) are usually associated with a Rubisco-containing micro-compartment, the pyrenoid. A link between the small subunit (SSU) of Rubisco and pyrenoid formation in Chlamydomonas reinhardtii has previously suggested that specific RbcS residues could explain pyrenoid occurrence in green algae. A phylogeny of RbcS was used to compare the protein sequence and CCM distribution across the green algae and positive selection in RbcS was estimated. For six streptophyte algae, Rubisco catalytic properties, affinity for CO2 uptake (K0.5 ), carbon isotope discrimination (δ13 C) and pyrenoid morphology were compared. The length of the βA-βB loop in RbcS provided a phylogenetic marker discriminating chlorophyte from streptophyte green algae. Rubisco kinetic properties in streptophyte algae have responded to the extent of inducible CCM activity, as indicated by changes in inorganic carbon uptake affinity, δ13 C and pyrenoid ultrastructure between high and low CO2 conditions for growth. We conclude that the Rubisco catalytic properties found in streptophyte algae have coevolved and reflect the strength of any CCM or degree of pyrenoid leakiness, and limitations to inorganic carbon in the aquatic habitat, whereas Rubisco in extant land plants reflects more recent selective pressures associated with improved diffusive supply of the terrestrial environment.

Highlights

Griffiths, Howard; Cambridge University, Department of Plant Science; Carbon concentrating mechanim (CCM), green algae, photosynthesis, pyrenoid, Rubisco, streptophyte algae iew Rubisco and carbon concentrating mechanism (CCM) co-evolution across Chlorophyte and Streptophyte green algae
Our expectation was based on (i) the observations that the RbcS -helices are important for pyrenoid formation in Chlamydomonas reinhardtii (Meyer et al, 2012), as well as (ii) recent in vitro and in vivo experiments showing that both small subunit (SSU) -helices are necessary and sufficient to interact with the Chlamydomonas Rubisco linker EPYC1 when expressed in heterologous systems (Atkinson et al, 2019)
Rubisco aggregation mechanisms may occur in more distantly related lineages, perhaps through interactions with the large subunit (LSU), which is the modus operandi in cyanobacterial carboxysomes (Oltrogge et al, 2019; Wang et al, 2019)

Summary

Introduction

Howard; Cambridge University, Department of Plant Science; Carbon concentrating mechanim (CCM), green algae, photosynthesis, pyrenoid, Rubisco, streptophyte algae iew Rubisco and carbon concentrating mechanism (CCM) co-evolution across Chlorophyte and Streptophyte green algae. Advanced Imaging Centre, University of Cambridge, Cambridge, CB2 3DY, UK; of Molecular Biology, Princeton University, Princeton, NJ 08544, USA

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