A protease-mediated mechanism regulates the cytochrome <i>c</i>₆/plastocyanin switch in <i>Synechocystis</i> sp. PCC 6803.

Abstract

After the Great Oxidation Event (GOE), iron availability was greatly decreased, and photosynthetic organisms evolved several alternative proteins and mechanisms. One of these proteins, plastocyanin, is a type I blue-copper protein that can replace cytochrome <i>c</i>₆ as a soluble electron carrier between cytochrome <i>b</i>₆<i>f</i> and photosystem I. In most cyanobacteria, expression of these two alternative proteins is regulated by copper availability, but the regulatory system remains unknown. Herein, we provide evidence that the regulatory system is composed of a BlaI/CopY-family transcription factor (PetR) and a BlaR-membrane protease (PetP). PetR represses <i>petE</i> (plastocyanin) expression and activates <i>petJ</i> (cytochrome <i>c</i>₆), while PetP controls PetR levels in vivo. Using whole-cell extracts, we demonstrated that PetR degradation requires both PetP and copper. Transcriptomic analysis revealed that the PetRP system regulates only four genes (<i>petE</i>, <i>petJ</i>, <i>slr0601</i>, and <i>slr0602</i>), highlighting its specificity. Furthermore, the presence of <i>petE</i> and <i>petRP</i> in early branching cyanobacteria indicates that acquisition of these genes could represent an early adaptation to decreased iron bioavailability following the GOE.