Study of Ecophysiological Responses of the Antarctic Fruticose Lichen Cladonia borealis Using the PAM Fluorescence System under Natural and Laboratory Conditions

Abstract

Antarctic lichens have been used as indicators of climate change for decades, but only a few species have been studied. We assessed the photosynthetic performance of the fruticose lichen Cladonia borealis under natural and laboratory conditions using the PAM fluorescence system. Compared to that of sun-adapted Usnea sp., the photosynthetic performance of C. borealis exhibits shade-adapted lichen features, and its chlorophyll fluorescence does not occur during dry days without rain. To understand its desiccation-rehydration responses, we measured changes in the PSII photochemistry in C. borealis under the average light intensity of dawn light and daylight and the desiccating conditions of its natural microclimate. Interestingly, samples under daylight and rapid-desiccation conditions showed a delayed reduction in Fv'/Fm' and rETRmax, and an increase in Y(II) and Y(NPQ) levels. These results suggest that the photoprotective mechanism of C. borealis depends on sunlight and becomes more efficient with improved desiccation tolerance. Amplicon sequencing revealed that the major photobiont of C. borealis was Asterochloris irregularis, which has not been reported in Antarctica before. Collectively, these results from both field and laboratory could provide a better understanding of specific ecophysiological responses of shade-adapted lichens in the Antarctic region.

Keywords: Antarctic; Cladonia borealis; desiccated state; fruticose lichens; non-photochemical quenching; phytochemistry; poikilohydric; shade-adapted lichen.

Figure 1

Location and landscape of the study site (KGL01: 62°14′24″ S, 58°44′36″ W), and an image of C. borealis at the field. (a) KGL01 on the map, placed near Potter Cove in Barton Peninsula. (b) This site has well-distinguished vegetation that consists of mosses and lichens. The area spanning the brown and grey parts was composed of lichens, and our observation was performed at the area indicated by the white box. (c) Several thalli of C. borealis accompanied by the moss Chorisdontium aciphyllum are shown.

Figure 2

Field observation of the fluorescence (F and Fm’) and Y(II) value of C. borealis and Usnea sp. and microclimate at the site. Grey shading indicates nighttime (10 PM to 4 AM) when photosynthetic photon flux density (PPFD) was less than 10 μmol/m²/s. (a,b) Fluorescence and Y(II) value of C. borealis (c,d) Fluorescence and Y(II) value of Usnea sp. Data were obtained from two individual thalli (Samples #1, #2). Patterns of fluorescence (F and Fm’) of C. borealis and Usnea sp. were similar between the two samples. (e) Changes in temperature (°C) and PPFD (μmol/m²/s). (f) Changes in volumetric soil moisture (%) and rainfall (mm) during the observation period. F, current fluorescence; Fm’, maximum fluorescence.

Figure 3

Correlation between Y(II) of C. borealis and PPFD (a), temperature (b), and volumetric soil moisture (c) parameters. Data were extracted from Regions A, B, and C in Figure 2b. A fitting analysis for linear regression was performed for each dataset. (d) The linear regression parameters are presented in a tabular format. Asterisks indicate R² > 0.5. SE, standard error.

Figure 4

Changes in maximal photosynthetic yield (Fv’/Fm’) (a,c) and rETRmax (b,d) with dawn-light (50 μmol/m²/s) and daytime-light (220 μmol/m²/s) under a desiccation-rehydration cycle in C. borealis. Before desiccation, samples were activated with light (50 μmol/m²/s) for 2 h under fully hydrated conditions with distilled water. The thalli were treated under slow desiccation (SD, 85% RH) (a,b) and rapid desiccation (RD, 5% RH) (c,d) for 24 h (until indicated by the dashed line), and then rehydrated with a water spray of distilled water (black arrow). After the removal of excess water, both samples were kept under SD conditions for an additional 2 h. The ten biological replicates were used for each treatment (n = 10). Experiments were repeated at least two or three times using the same thalli after re-stabilizing at 50 μmol/m²/s light with an 18:6 light:dark cycle at 8 °C with hydration for a week. Results are the means with ± standard deviation shown by vertical bars.

Figure 5

PSII photochemistry changes during RLC experiments under the given conditions. (a) Effective photosynthetic yield Y(II), (b) 1-qP value, and (c) Y(NPQ)/Y(NO) ratio. Each value indicates the average score ± standard deviation, calculated from the data in Figure S6. The average was calculated by two-way ANOVA, and its significant differences among the data were analyzed based on the Tukey’s HSD test (at p < 0.05) which was displayed with different letters; upper case letters indicate the effects of light intensity at the same time of desiccation (or rehydration) treatment, and lower case letters indicate the effects of desiccation (or rehydration) treatment at the same light condition. The ten biological replicates were used for each treatment (n = 10). Experiments were repeated at least two or three times using the same thalli after re-stabilizing at 50 μmol/m²/s light with an 18:6 light:dark cycle at 8 °C with hydration for a week. Black and red bars represent dawn light (50 μmol/m²/s) and daylight (220 μmol/m²/s), respectively. Y(NPQ), the efficiency of the regulated non-photochemical quenching reaction; Y(NO), the efficiency of the nonregulated non-photochemical quenching reaction; SD, slow desiccation; RD, rapid desiccation; RD→Rehyd., rehydration after 24 h of RD treatment.