Dissecting the Photoprotective Mechanism Encoded by the flv4‐2 Operon: a Distinct Contribution of Sll0218 in Photosystem II Stabilization

Abstract

In Synechocystis sp. PCC 6803, the flv4-2 operon encodes the flavodiiron proteins Flv2 and Flv4 together with a small protein, Sll0218, providing photoprotection for Photosystem II (PSII). Here, the distinct roles of Flv2/Flv4 and Sll0218 were addressed, using a number of flv4-2 operon mutants. In the Δsll0218 mutant, the presence of Flv2/Flv4 rescued PSII functionality as compared with Δsll0218-flv2, where neither Sll0218 nor the Flv2/Flv4 heterodimer are expressed. Nevertheless, both the Δsll0218 and Δsll0218-flv2 mutants demonstrated deficiency in accumulation of PSII proteins suggesting a role for Sll0218 in PSII stabilization, which was further supported by photoinhibition experiments. Moreover, the accumulation of PSII assembly intermediates occurred in Sll0218-lacking mutants. The YFP-tagged Sll0218 protein localized in a few spots per cell at the external side of the thylakoid membrane, and biochemical membrane fractionation revealed clear enrichment of Sll0218 in the PratA-defined membranes, where the early biogenesis steps of PSII occur. Further, the characteristic antenna uncoupling feature of the Δflv4-2 operon mutants is shown to be related to PSII destabilization in the absence of Sll0218. It is concluded that the Flv2/Flv4 heterodimer supports PSII functionality, while the Sll0218 protein assists PSII assembly and stabilization, including optimization of light harvesting.

Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light

“…PCC7120 (hereafter Synechocystis and Anabaena , respectively) under FL (Allahverdiyeva et al ., ). Another cyanobacterial FDP heterodimer, encoded by the flv4‐2 operon, has been shown to be active in the photoprotection of PSII (Zhang et al ., ; Bersanini et al ., , ). Genes encoding proteins with high homology to cyanobacterial Flv1 and Flv3 are present in non‐vascular plants and in gymnosperms, but were lost during evolution in flowering plants (Allahverdiyeva et al ., ; Ilík et al ., ).…”

The Fluctuating Cell-Specific Light Environment and Its Effects on Cyanobacterial Physiology

“…The mechanisms include two respiratory terminal oxidases, and flavodiiron (flv) proteins. Flv protein can operate either to maintain function of PSII (Bersanini et al, 2014(Bersanini et al, , 2017 or to divert electrons downstream of PSI (Allahverdiyeva et al, 2013). Despite a growing understanding of the molecular complexity of cyanobacterial photoprotection under various laboratory light regimes, very little is known about how these mechanisms operate under complex natural or industrially relevant light conditions.…”

A Carbon Dioxide Limitation-Inducible Protein, ColA, Supports the Growth of Synechococcus sp. PCC 7002

“…For example, S. 6803 harbors sll0218 as a ColA gene, whereas S. 7942 has no gene encoding ColA. The gene sll0218 in S. 6803 is highly expressed under CO 2 -limited conditions, like that observed for SYNPCC7002_A2492 in S. 7002 [ 16 ], and is proposed to stabilize PSII [ 28 ]. We aligned the amino acid sequences of ColA isozymes in S. 7002 and S. 6803 ( Supplemental Figure S2 ) and found a 68% similarity between the primary structures of these gene products in the ClustalW analysis.…”

“…We aligned the amino acid sequences of ColA isozymes in S. 7002 and S. 6803 ( Supplemental Figure S2 ) and found a 68% similarity between the primary structures of these gene products in the ClustalW analysis. We constructed the phylogenetic tree of ColA isozymes based on amino acid sequences of some cyanobacteria ( Figure 6 ), which indicated that the genes for ColA are normally encoded between the genes for FLV4 and FLV2, designated the flv4-2 operon, by Aro’ and colleagues, in cyanobacterial genomes [ 16 , 28 ]. In fact, all the cyanobacteria species registered in CyanoBase [ 29 ] possess genes for FLV2/4, similar to S. 6803, with S. 7002 as the only exception ( Figure 6 ).…”