Abstract
Sulphide is proposed to have influenced the evolution of primary stages of oxygenic photosynthesis in cyanobacteria. However, sulphide is toxic to most of the species of this phylum, except for some sulphide-tolerant species showing various sulphide-resistance mechanisms. In a previous study, we found that this tolerance can be induced by environmental sulphidic conditions, in which two experimentally derived strains with an enhanced tolerance to sulphide were obtained from Microcystis aeruginosa, a sensitive species, and Oscillatoria, a sulphide-tolerant genus. We have now analysed the photosynthetic performance of the wild-type and derived strains in the presence of sulphide to shed light on the characteristics underlying the increased tolerance. We checked whether the sulphide tolerance was a result of higher PSII sulphide resistance and/or the induction of sulphide-dependent anoxygenic photosynthesis. We observed that growth, maximum quantum yield, maximum electron transport rate and photosynthetic efficiency in the presence of sulphide were less affected in the derived strains compared to their wild-type counterparts. Nevertheless, in 14C photoincoporation assays, neither Oscillatoria nor M. aeruginosa exhibited anoxygenic photosynthesis using sulphide as an electron donor. On the other hand, the content of photosynthetic pigments in the derived strains was different to that observed in the wild-type strains. Thus, an enhanced PSII sulphide resistance appears to be behind the increased sulphide tolerance displayed by the experimentally derived strains, as observed in most natural sulphide-tolerant cyanobacterial strains. However, other changes in the photosynthetic machinery cannot be excluded.
Highlights
Because oxygenic photosynthesis seems to have evolved in cyanobacteria-like organisms living in sulphide-rich waters (Canfield 1998; Battistuzzi et al 2004), sulphide is proposed to have influenced the primary stages of the evolution of oxygenic photosynthesis
Cohen et al (1986) classified cyanobacteria according to the PSI and PSII sulphide-tolerance level and the capacity for performing anoxygenic photosynthesis using H2S as an e− donor: (i) cyanobacteria with sulphide-sensitive oxygenic photosynthesis; (ii) species with sulphideresistant oxygenic photosynthesis; (iii) cyanobacteria with sulphide-resistant oxygenic photosynthesis, more sensitive than type (ii), concurrent with the partial induction of sulphide-dependent anoxygenic photosynthesis; and (iv) cyanobacteria in which H 2S-dependent anoxygenic photosynthesis replaces oxygenic photosynthesis at high sulphide concentrations
We found that the derived experimental populations significantly increased the initial sulphide tolerance observed in their ancestors, as these derived populations of M. aeruginosa and Oscillatoria sp. were able to grow at 0.4 and 2 mM sulphide, respectively (Martín-Clemente et al 2019)
Summary
Because oxygenic photosynthesis seems to have evolved in cyanobacteria-like organisms living in sulphide-rich waters (Canfield 1998; Battistuzzi et al 2004), sulphide is proposed to have influenced the primary stages of the evolution of oxygenic photosynthesis. The main objective of our study was to analyse the changes in photosynthetic performance of the derived, experimental strains, to check whether their increased sulphide tolerance could be due to a higher PSII sulphide resistance and/or the induction of sulphide-dependent photosynthesis, especially in Oscillatoria. For this purpose, the effect of sulphide on the maximum quantum yield of PSII and the electron transport rate under different sulphide concentrations was analysed and compared between derived and wild-type strains, as well as the effect of sulphide on their growth rates. To shed more light on the process of tolerance acquisition, we analysed if adaptation or acclimation was the mechanism involved in this process and its possible physiological cost in terms of growth and photosynthetic rates
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