Computational Analysis of Alternative Photosynthetic Electron Flows Linked With Oxidative Stress.

Nima P Saadat,Tim Nies,Marvin Van Aalst,Brandon Hank,Oliver Ebenhöh,Büsra Demirtas,Anna Matuszyńska

doi:10.3389/fpls.2021.750580

Abstract

During photosynthesis, organisms respond to their energy demand and ensure the supply of energy and redox equivalents that sustain metabolism. Hence, the photosynthetic apparatus can, and in fact should, be treated as an integrated supply-demand system. Any imbalance in the energy produced and consumed can lead to adverse reactions, such as the production of reactive oxygen species (ROS). Reaction centres of both photosystems are known sites of ROS production. Here, we investigate in particular the central role of Photosystem I (PSI) in this tightly regulated system. Using a computational approach we have expanded a previously published mechanistic model of C3 photosynthesis by including ROS producing and scavenging reactions around PSI. These include two water to water reactions mediated by Plastid terminal oxidase (PTOX) and Mehler and the ascorbate-glutathione (ASC-GSH) cycle, as a main non-enzymatic antioxidant. We have used this model to predict flux distributions through alternative electron pathways under various environmental stress conditions by systematically varying light intensity and enzymatic activity of key reactions. In particular, we studied the link between ROS formation and activation of pathways around PSI as potential scavenging mechanisms. This work shines light on the role of alternative electron pathways in photosynthetic acclimation and investigates the effect of environmental perturbations on PSI activity in the context of metabolic productivity.

Highlights

Photosynthetic organisms are the primary producers of biomass available in the biosphere
Embedded in the thylakoid membrane, the photosynthetic electron transport chain (PETC) mediates the transfer of electrons, extracted from water molecules, over the complexes of Photosystem II (PSII), Cytochromeb6f, and Photosystem I (PSI) to the final electron acceptor NADP+ via the mobile electron carriers plastoquinone (PQ), plastocyanin (PC), and ferredoxin (Fd)
The transition to the lightsaturated regime occurs around a photosynthetic photon flux density (PPFD) of 900 μmol m−2s−1, which is in good agreement with previously observed and modelled values (Kromdijk et al, 2019)

Summary

Introduction

Photosynthetic organisms are the primary producers of biomass available in the biosphere. By employing complex biophysical processes, which act on multiple temporal and spatial scales, they perform highly efficient energy converting reactions (see for example Ksenzhek and Volkov, 1998). The second part of the photosynthetic process is the Calvin-Benson-Bassham (CBB) cycle, regulated by the Electron Flows Around PSI thioredoxin system (Geigenberger et al, 2017). NADPH and ATP produced by the PETC are used during the CBB cycle to fix CO2 into organic compounds. Any imbalance between production and consumption can lead to adverse reactions, such as the production of reactive oxygen species (ROS) (Asada, 2006; Suzuki et al, 2012; Schwarzlander and Finkemeier, 2013) and affect the overall photosynthetic efficiency. Several sub-processes exist, distributed over the whole PETC, that contribute to the production of potentially toxic ROS compounds (Maurino and Flügge, 2008; Dietz et al, 2016; Khorobrykh et al, 2020)

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