Exploring the Diversity of the Thioredoxin Systems in Cyanobacteria

Abstract

Cyanobacteria evolved the ability to perform oxygenic photosynthesis using light energy to reduce CO2 from electrons extracted from water and form nutrients. These organisms also developed light-dependent redox regulation through the Trx system, formed by thioredoxins (Trxs) and thioredoxin reductases (TRs). Trxs are thiol-disulfide oxidoreductases that serve as reducing substrates for target enzymes involved in numerous processes such as photosynthetic CO2 fixation and stress responses. We focus on the evolutionary diversity of Trx systems in cyanobacteria and discuss their phylogenetic relationships. The study shows that most cyanobacteria contain at least one copy of each identified Trx, and TrxA is the only one present in all genomes analyzed. Ferredoxin thioredoxin reductase (FTR) is present in all groups except Gloeobacter and Prochlorococcus, where there is a ferredoxin flavin-thioredoxin reductase (FFTR). Our data suggest that both TRs may have coexisted in ancestral cyanobacteria together with other evolutionarily related proteins such as NTRC or DDOR, probably used against oxidative stress. Phylogenetic studies indicate that they have different evolutionary histories. As cyanobacteria diversified to occupy new habitats, some of these proteins were gradually lost in some groups. Finally, we also review the physiological relevance of redox regulation in cyanobacteria through the study of target enzymes.

Back to the future: Transplanting the chloroplast TrxF–FBPase–SBPase redox system to cyanobacteria

“…This suggests that Trx f could have a chaperone function as it has been suggested before (Sanz-Barrio et al, 2012;Du et al, 2015). Our results also show that, despite the plant proteins introduced in this work are not present in Synechocystis (or any other cyanobacteria) and have a different evolutionary origin in all three cases (Sahrawy et al, 1996;Capitani et al, 2000;Gütle et al, 2016;Malleń-Ponce et al, 2022), it can be reduced by the cyanobacterial FTR-Trx system. These results suggest that, when these proteins were acquired by the primitive photosynthetic eukaryote, they could be reduced by the chloroplast redox-reducing system.…”

“…In addition, in recent years, it has been described that thioredoxin target proteins are oxidized in the dark by Trx-like proteins and Trxs themselves, which ultimately donate their electrons to H 2 O 2 though NTRC and 2cys-prx ( Balsera and Buchanan, 2019 ; Yoshida et al., 2019 ; Yokochi et al., 2021 ). Although NTRC and 2cys-prx are present in many cyanobacteria, NTRC is not present in Synechocystis ( Mallén-Ponce et al., 2022 ), and the 2cys-prx from Synechocystis presents different biochemical characteristics to the plant enzyme ( Pascual et al., 2010 ; Pascual et al., 2011 ). Cyanobacteria also lack Trx-like proteins that are essential for oxidation in the dark, and, therefore, this might explain why thioredoxin targets are less oxidized in cyanobacteria.…”

“…Most cyanobacteria also contain an additional enzyme that only exhibits FBPase activity ( Udvardy et al., 1982 ; Tamoi et al., 1996 ; Tamoi et al., 1998 ; Tamoi et al., 1999 ; Nakahara et al., 2003 ). Cyanobacterial proteins have a different evolutionary origin to plant FBPase and SBPase ( Jiang et al., 2012 ; Gütle et al., 2016 ), which were acquired later during plant evolution ( Sahrawy et al., 1996 ; Capitani et al., 2000 ; Jiang et al., 2012 ; Gütle et al., 2016 ; Mallén-Ponce et al., 2022 ).…”

“…Thioredoxins are small redox proteins (~12 kDa) that have been found in all organisms ( Schürmann and Buchanan, 2008 ; Balsera and Buchanan, 2019 ) and are capable of reducing disulfide bridges in other proteins. The plant FTR-Trx system has a cyanobacterial origin and with most of its components [FTR, Trx m , Trx x , Trx y , and NADPH thioredoxin reductase C (NTRC)] being present in cyanobacteria ( Buchanan, 2016 ; Geigenberger et al., 2017 ; Mallén-Ponce et al., 2022 ).…”

SynDLP is a dynamin-like protein of Synechocystis sp. PCC 6803 with eukaryotic features

“…Thus, it can be assumed that a disulfide bridge-stabilized BSE domain is a general feature observable in this clade of cyanobacterial DLPs. In fact, several proteins in the cyanobacterial cytoplasm contain disulfide bridges, and the (in part reversible) formation of disulfide bridges is mediated by the thioredoxin system [68][69][70] . Thus, it might even be possible that a reversible formation of the disulfide bridge in the BSE domain is involved in the regulation of the SynDLP activity.…”