Complementary UV-absorption of mycosporine-like amino acids and scytonemin is responsible for the UV-insensitivity of photosynthesis in Nostoc flagelliforme

Abstract

Mycosporine-like amino acids (MAAs) and scytonemin are UV-screening compounds that have presumably appeared early in the history of life and are widespread in cyanobacteria. Natural colonies of the UV-insensitive Nostoc flagelliforme were found to be especially rich in MAAs (32.1 mg g DW(-1)), concentrated in the glycan sheath together with scytonemin. MAAs are present in the form of oligosaccharide-linked molecules. Photosystem II activity, measured using PAM fluorescence and oxygen evolution, was used as a most sensitive physiological parameter to analyse the effectiveness of UV-protection. Laboratory experiments were performed under controlled conditions with a simulated solar radiation specifically deprived of UV-wavebands with cut-off filters (295, 305, 320, 345 and 395 nm). The UV-insensitivity of N. flagelliforme was found to cover the whole UV-A (315-400 nm) and UV-B (280-320 nm) range and is almost certainly due to the complementary UV-absorption of MAAs and scytonemin. The experimental approach used is proposed to be suitable for the comparison of the UV-protection ability in organisms that differ in their complement of UV-sunscreen compounds. Furthermore, this study performed with a genuinely terrestrial organism points to the relevance of marine photoprotective compounds for life on Earth, especially for the colonization of terrestrial environments.

Keywords: Nostoc flagelliforme; UV-radiation; mycosporine-like amino acids; photosynthesis; scytonemin.

Figure 1

(a) Absorption spectrum of an extract from N. flagelliforme in 80% tetrahydrofuran. (b–c) Micrographs of sections (10 μm thick) of N. flagelliforme showing the peripheral localization of yellow-brown scytonemin. Scale bar: 50 μm. Longitudinal section (b); cross section (c).

Figure 2

(a) Absorption spectrum of an extract from N. flagelliforme in 20% methanol. (b) Chromatogram of UV-absorbing putative OS-MAAs from N. flagelliforme. Lichrospher RP-18 (5 μ, 250*4 mm I.D), 1 mL min⁻¹, 0–15 min: 100% A (0.02% acetic acid in water). 15–30 min: linear increase from 0% B (acetonitrile) to 20% B.

Figure 3

Non-photochemical quenching (NPQ, continuous lines) and photochemical quenching (qP, broken lines) of chlorophyll fluorescence in N. flagelliforme (closed circles) and N. commune (open circles) under increasing light intensity.

Figure 4

PS II quantum yield during exposure of N. flagelliforme (a) and N. commune (b) to a solar lamp using different cut-off filters (indicated in the legend). The shaded areas indicate recovery times after transfer to dim light. Each point represents the mean ±SD (n = 4–5).

Figure 5

Linear regression of the initial recovery rate of PSII yield after transfer to dim light with the cut-off wavelength of the filters used during simulated solar irradiation.

Figure 6

Oxygen evolution of N. flagelliforme (a) and N. commune (b) during exposure to a solar lamp either deprived of the UV-components of its spectrum (PAR) or not (PAR + UV). Each point represents mean ±SD (n = 4–5).