Abstract
The FUR (Ferric Uptake Regulator) family in Anabaena sp. PCC 7120 consists of three paralogs named FurA (Fur), FurB (Zur) and FurC (PerR). furC seems to be an essential gene in the filamentous nitrogen-fixing strain Anabaena sp. PCC 7120, suggesting that it plays a fundamental role in this organism. In order to better understand the functions of FurC in Anabaena, the phenotype of a derivative strain that overexpresses this regulator (EB2770FurC) has been characterized. The furC-overexpressing variant presented alterations in growth rate, morphology and ultrastructure, as well as higher sensitivity to peroxide than Anabaena sp. PCC 7120. Interestingly, the overexpression of furC led to reduced photosynthetic O2 evolution, increased respiratory activity, and had a significant influence in the composition and efficiency of both photosystems. Comparative transcriptional analyses, together with electrophoretic mobility shift assays allowed the identification of different genes directly controlled by FurC, and involved in processes not previously related to PerR proteins, such as the cell division gene ftsZ and the major thylakoid membrane protease ftsH. The rise in the transcription of ftsH in EB2770FurC cells correlated with reduced levels of the D1 protein, which is involved in the PSII repair cycle. Deregulation of the oxidative stress response in EB2770FurC cells led to the identification of novel FurC targets involved in the response to H2O2 through different mechanisms. These results, together with the effect of furC overexpression on the composition, stability and efficiency of the photosynthetic machinery of Anabaena, disclose novel links between PerR proteins, cell division and photosynthesis in filamentous cyanobacteria.
Highlights
Cyanobacteria contain a unique combination of light-harvesting complexes composed by membrane-bound antenna present in both photosystems and by phycobilisomes bound to the surface of the thylakoid membrane that transfer light energy to chlorophyll a (Chl a)
Non-diazotrophic cyanobacterium Synechocystis PCC 6803, PerR is encoded by slr1738, and its disruption allowed the identification of a putative regulon that includes about 37 genes mainly involved in the oxidative stress response, transport across membranes, iron metabolism and CO2 concentration (Kobayashi et al 2004; Li et al 2004)
In the light of these results, we investigated the potential involvement of FurC in the modulation of some of the genes related to morphology and growth processes such as the the mreBCD operon, encoding the bacterial actins MreB, MreC and MreD (Hu et al 2007), responsible for changes in cell morphology, as well as the cell division genes ftsZ and ftsH
Summary
Cyanobacteria contain a unique combination of light-harvesting complexes composed by membrane-bound antenna present in both photosystems and by phycobilisomes bound to the surface of the thylakoid membrane that transfer light energy to chlorophyll a (Chl a). Among transition metals, iron is the major cofactor needed for photosynthesis but for other cyanobacterial electron transport pathways involved in respiration, oxidative phosphorylation and nitrate assimilation. In Anabaena, photosynthesis, respiration, nitrogen metabolism and the oxidative stress response are tightly related to metal homeostasis and are coordinately regulated mainly by FUR (Ferric Uptake Regulator) proteins (Gonzalez et al 2010; Gonzalez et al 2016; Lopez-Gomollon et al 2007; Sein-Echaluce et al 2015). Non-diazotrophic cyanobacterium Synechocystis PCC 6803, PerR is encoded by slr1738, and its disruption allowed the identification of a putative regulon that includes about 37 genes mainly involved in the oxidative stress response, transport across membranes, iron metabolism and CO2 concentration (Kobayashi et al 2004; Li et al 2004). Our results unveil that the expression levels of FurC in Anabaena are related to the control of cell-growth parameters as well as to the composition and efficiency of the photosynthetic machinery
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