Redox-coupled proton pumping drives carbon concentration in the photosynthetic complex I

Ville R I Kaila,Jan M Schuller,Genji Kurisu,Marc M Nowaczyk,Jacqueline Thiemann,Sandra K Schuller,Ana P Gamiz-Hernandez,Patricia Saura

doi:10.1038/s41467-020-14347-4

Abstract

Photosynthetic organisms capture light energy to drive their energy metabolism, and employ the chemical reducing power to convert carbon dioxide (CO2) into organic molecules. Photorespiration, however, significantly reduces the photosynthetic yields. To survive under low CO2 concentrations, cyanobacteria evolved unique carbon-concentration mechanisms that enhance the efficiency of photosynthetic CO2 fixation, for which the molecular principles have remained unknown. We show here how modular adaptations enabled the cyanobacterial photosynthetic complex I to concentrate CO2 using a redox-driven proton-pumping machinery. Our cryo-electron microscopy structure at 3.2 Å resolution shows a catalytic carbonic anhydrase module that harbours a Zn2+ active site, with connectivity to proton-pumping subunits that are activated by electron transfer from photosystem I. Our findings illustrate molecular principles in the photosynthetic complex I machinery that enabled cyanobacteria to survive in drastically changing CO2 conditions.

Highlights

Photosynthetic organisms capture light energy to drive their energy metabolism, and employ the chemical reducing power to convert carbon dioxide (CO2) into organic molecules
Cyanobacteria evolved around 2.7 billion years ago with the ability to oxidise water into dioxygen (O2) using the energy captured from sunlight[1]
The light-driven water splitting catalysed by photosystem II (PSII), reduces plastoquinone (PQ) and establishes an electrochemical proton gradient across the thylakoid membrane that subsequently drives synthesis of adenosine triphosphate (ATP)[3,4]

Summary

Introduction

Photosynthetic organisms capture light energy to drive their energy metabolism, and employ the chemical reducing power to convert carbon dioxide (CO2) into organic molecules. To survive under low CO2 concentrations, cyanobacteria evolved unique carbon-concentration mechanisms that enhance the efficiency of photosynthetic CO2 fixation, for which the molecular principles have remained unknown. During linear electron flow (LEF), the electrons are transferred to photosystem I (PSI), providing the reducing power for photosynthetic CO2 fixation that consumes nicotinamide adenine dinucleotide phosphate (NADPH) and drives the synthesis of complex organic compounds from inorganic carbon (Ci)[2]. The HCO3− subsequently diffuses into the carboxysome micro-compartments, where it is converted by a carboxysomal CA to CO27, which further carboxylates ribulose-1,5-bisphosphate (RuBP) into carbohydrates by the action of RuBisCO (Ribulose-1,5-bisphosphate carboxylase/oxygenase)[10] This CCM of the photosynthetic complex I, prevents CO2 to diffuse out of the cell by concentrating the Ci for RuBisCO, providing a basis for the efficient carbon fixation that is hampered during photorespiration[7]. To determine the molecular architecture of NDH-1MS (NDH13), we isolate the enzyme from the cyanobacterium Thermosynechococcus elongatus, solved its molecular structure at 3.2 Å resolution using cryo-EM (Fig. 1, Supplementary Fig. 1, Supplementary Table 1, and Supplementary Movie 1), and probe its molecular mechanism by classical and quantum mechanical simulations

Methods

Results

Conclusion