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Antenna proton sensitivity determines photosynthetic light harvesting strategy.

ABSTRACT: Photoprotective non-photochemical quenching (NPQ) represents an effective way to dissipate the light energy absorbed in excess by most phototrophs. It is often claimed that NPQ formation/relaxation kinetics are determined by xanthophyll composition. We, however, found that, for the alveolate alga Chromera velia, this is not the case. In the present paper, we investigated the reasons for the constitutive high rate of quenching displayed by the alga by comparing its light harvesting strategies with those of a model phototroph, the land plant Spinacia oleracea. Experimental results and in silico studies support the idea that fast quenching is due not to xanthophylls, but to intrinsic properties of the Chromera light harvesting complex (CLH) protein, related to amino acid composition and protein folding. The pKa for CLH quenching was shifted by 0.5 units to a higher pH compared with higher plant antennas (light harvesting complex II; LHCII). We conclude that, whilst higher plant LHCIIs are better suited for light harvesting, CLHs are 'natural quenchers' ready to switch into a dissipative state. We propose that organisms with antenna proteins intrinsically more sensitive to protons, such as C. velia, carry a relatively high concentration of violaxanthin to improve their light harvesting. In contrast, higher plants need less violaxanthin per chlorophyll because LHCII proteins are more efficient light harvesters and instead require co-factors such as zeaxanthin and PsbS to accelerate and enhance quenching.

SUBMITTER: Kuthanova Trskova E

PROVIDER: S-EPMC6093471 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Antenna proton sensitivity determines photosynthetic light harvesting strategy.

Kuthanová Trsková Eliška E Belgio Erica E Yeates Anna M AM Sobotka Roman R Ruban Alexander V AV Kana Radek R

Journal of experimental botany 20180801 18

Photoprotective non-photochemical quenching (NPQ) represents an effective way to dissipate the light energy absorbed in excess by most phototrophs. It is often claimed that NPQ formation/relaxation kinetics are determined by xanthophyll composition. We, however, found that, for the alveolate alga Chromera velia, this is not the case. In the present paper, we investigated the reasons for the constitutive high rate of quenching displayed by the alga by comparing its light harvesting strategies wit ...[more]

PMID: 29955883

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Project description:Many photosynthetic bacteria have peripheral light-harvesting (LH) antenna complexes that increase the efficiency of light energy capture. The purple nonsulfur photosynthetic bacterium Rhodopseudomonas palustris produces different types of LH complexes under high light intensities (LH2 complex) and low light intensities (LH3 and LH4 complexes). There are multiple pucBA operons that encode the ? and ? peptides that make up these complexes. However, low-resolution structures, amino acid similarities between the complexes, and a lack of transcription analysis have made it difficult to determine the contributions of different pucBA operons to the composition and function of different LH complexes. It was also unclear how much diversity of LH complexes exists in R. palustris and affiliated strains. To address this, we undertook an integrative genomics approach using 20 sequenced strains. Gene content analysis revealed that even closely related strains have differences in their pucBA gene content. Transcriptome analyses of the strains grown under high light and low light revealed that the patterns of expression of the pucBA operons varied among strains grown under the same conditions. We also found that one set of LH2 complex proteins compensated for the lack of an LH4 complex under low light intensities but not under extremely low light intensities, indicating that there is functional redundancy between some of the LH complexes under certain light intensities. The variation observed in LH gene composition and expression in Rhodopseudomonas strains likely reflects how they have evolved to adapt to light conditions in specific soil and water microenvironments. IMPORTANCERhodopseudomonas palustris is a phototrophic purple nonsulfur bacterium that adapts its photosystem to allow growth at a range of light intensities. It does this by adjusting the amount and composition of peripheral light-harvesting (LH) antenna complexes that it synthesizes. Rhodopseudomonas strains are notable for containing numerous sets of light-harvesting genes. We determined the diversity of LH complexes and their transcript levels during growth under high and low light intensities in 20 sequenced genomes of strains related to the species Rhodopseudomonas palustris. The data obtained are a resource for investigators with interests as wide-ranging as the biophysics of photosynthesis, the ecology of phototrophic bacteria, and the use of photosynthetic bacteria for biotechnology applications.

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Antenna proton sensitivity determines photosynthetic light harvesting strategy.

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Antenna proton sensitivity determines photosynthetic light harvesting strategy.

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