Early emergence of the FtsH proteases involved in photosystem II repair

S Shao,T Cardona,P J Nixon

doi:10.1007/s11099-018-0769-9

Abstract

Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair form a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of photosynthetic water oxidation chemistry.

Highlights

Oxygenic photosynthetic electron transport from water to NADP+ requires the participation of two functionally distinct reactions centers (RCs) acting in series: photosystem II (PSII, a Type II RC containing quinone electron acceptors) and photosystem I (PSI, a Type I RC containing redox-active iron-sulphur clusters)
Ideas on the emergence of oxygenic photosynthesis focused on the evolution of PSI and PSII from pre-existing RC found in anoxygenic photosynthetic bacteria (Nitschke and Rutherford 1991) and the horizontal transfer of genes encoding chlorophyll biosynthetic enzymes and RC proteins (Hohmann-Marriott and Blankenship 2011, Fischer et al 2016)
More recent phylogenetic analyses have led to the suggestion that the evolution of Type I and Type II RCs might have occurred in a single organism after a gene duplication event (Mulkidjanian et al 2006, Sousa et al 2013, Harel et al 2015) and, possibly, that Type I and Type II RCs might have been transferred at various stages of evolution to other types of nonphotosynthetic bacteria through horizontal gene transfer (HGT)

Summary

Introduction

Oxygenic photosynthetic electron transport from water to NADP+ requires the participation of two functionally distinct reactions centers (RCs) acting in series: photosystem II (PSII, a Type II RC containing quinone electron acceptors) and photosystem I (PSI, a Type I RC containing redox-active iron-sulphur clusters). Ideas on the emergence of oxygenic photosynthesis focused on the evolution of PSI and PSII from pre-existing RC found in anoxygenic photosynthetic bacteria (Nitschke and Rutherford 1991) and the horizontal transfer of genes encoding chlorophyll biosynthetic enzymes and RC proteins (Hohmann-Marriott and Blankenship 2011, Fischer et al 2016). Because existing anoxygenic photosynthetic bacteria contain just one type of RC, such ‘gene acquisition’ hypotheses require at least two bacterial ancestors: one providing a Type II RC and another a Type I RC. Phylogenetic attempts (Sakamoto et al 2003, Yu et al 2004, Yu 2005) using a limited sequence dataset suggested that the FtsH subunits required for PSII repair exist in two main forms, denoted Type A and Type B (Zaltsman et al 2005). The evolutionary relationship between these FtsH subunits and the others found in nature remains poorly understood

Methods

Results

Conclusion