Light and Dehydration but Not Temperature Drive Photosynthetic Adaptations of Basal Streptophytes (Hormidiella, Streptosarcina and Streptofilum) Living in Terrestrial Habitats

Abstract

Streptophyte algae are the ancestors of land plants, and several classes contain taxa that are adapted to an aero-terrestrial lifestyle. In this study, four basal terrestrial streptophytes from the class Klebsormidiophyceae, including Hormidiella parvula; two species of the newly described genus Streptosarcina (S. costaricana and S. arenaria); and the newly described Streptofilum capillatum were investigated for their responses to radiation, desiccation and temperature stress conditions. All the strains showed low-light adaptation (I_k < 70 μmol photons m^-2 s^-1) but differed in photoprotective capacities (such as non-photochemical quenching). Acclimation to enhanced photon fluence rates (160 μmol photons m^-2 s^-1) increased photosynthetic performance in H. parvula and S. costaricana but not in S. arenaria, showing that low-light adaptation is a constitutive trait for S. arenaria. This lower-light adaptation of S. arenaria was coupled with a higher desiccation tolerance, providing further evidence that dehydration is a selective force shaping species occurrence in low light. For protection against ultraviolet radiation, all species synthesised and accumulated different amounts of mycosporine-like amino acids (MAAs). Biochemically, MAAs synthesised by Hormidiella and Streptosarcina were similar to MAAs from closely related Klebsormidium spp. but differed in retention time and spectral characteristics in S. capillatum. Unlike the different radiation and dehydration tolerances, Hormidiella, Streptosarcina and Streptofilum displayed preferences for similar thermal conditions. These species showed a temperature dependence of photosynthesis similar to respiration, contrasting with Klebsormidium spp. and highlighting an interspecific diversity in thermal requirements, which could regulate species distributions under temperature changes.

Keywords: Acclimation; Desiccation; Green algae; Photoprotection; Streptophyta; Temperature.

Fig. 1

Photosynthetic response to irradiance (RLC curves) of Hormidiella parvula, Streptosarcina costaricana and Streptosarcina arenaria strains SAG 2562 and SAG 2560 cultured in control (CL; 60 μmol photons (PAR) m⁻² s⁻¹) and moderate [ML; 160 μmol photons (PAR) m⁻² s⁻¹] photon fluence rates. Vertical bars indicate standard deviations of at least three independent culture replicates

Fig. 2

NPQ kinetics of Hormidiella parvula and Streptosarcina arenaria strains SAG 2562 and SAG 2560, Streptosarcina costaricana and Streptofilum capillatum cultured in control [CL; 60 μmol photons (PAR) m⁻² s⁻¹] and moderate [ML; 160 μmol photons (PAR) m⁻² s⁻¹] photon fluence rates. NPQ of S. capillatum under ML could not be determined, as the cultures died during the light-acclimation experiment. Arrow indicates the transient NPQ relaxation in the light. Data are from at least three culture replicates. Standard deviations are not shown

Fig. 3

Changes in effective quantum yield (YII) during dehydration followed by rehydration with stock culture medium. a, b Results for dehydration and recovery of Streptosarcina arenaria strains SAG 2562 and SAG 2560. c Results for dehydration of Hormidiella parvula, Streptosarcina costaricana and Streptofilum capillatum. d No recovery of H. parvula, S. costaricana and S. capillatum after rehydration. Values are reported as mean of at least three independent measurements ± SD

Fig. 4

Rapid thermal responses of gross photosynthesis (P) and respiration (R) for the species studied. At 45 °C, gross P was completely suppressed for Hormidiella parvula, Streptosarcina arenaria SAG 2560, Streptosarcina costaricana and Streptofilum capillatum. Measurements were performed on at least three independent culture replicates

Fig. 5

a Respiration (R) to gross photosynthesis (P) ratios as function of increasing temperature. b Comparison between activation energies for gross photosynthesis (E_a P) and respiration (E_a R) for Hormidiella, Streptosarcina and Streptofilum. c Comparison of activation energies measured for Klebsormidium spp. and calculated from results reported by Karsten et al. [16, 60]. Asterisks indicate statistically significant differences of E_a R in comparison to E_a P. Values are calculated from at least three independent measurements