Ultraviolet radiation and the snow alga Chlamydomonas nivalis (Bauer) Wille[para]

Photochemistry and Photobiology, Jun 2003 by Gorton, Holly L, Vogelmann, Thomas C

ABSTRACT

Aplanospores of Chlamydomonas nivalis are frequently found in high-altitude, persistent snowfields where they are photosynthetically active despite cold temperatures and high levels of visible and ultraviolet (UV) radiation. The goals of this work were to characterize the UV environment of the cells in the snow and to investigate the existence and localization of screening compounds that might prevent UV damage. UV irradiance decreased precipitously in snow, with UV radiation of wavelengths 280-315 nm and UV radiation of wavelengths 315-400 nm dropping to 50% of incident levels in the top 1 and 2 cm, respectively. Isolated cell walls exhibited UV absorbance, possibly by sporopollenin, but this absorbance was weak in images of broken or plasmolyzed cells observed through a UV microscope. The cells also contained UV-absorbing cytoplasmic compounds, with the extrachloroplastic carotenoid astaxanthin providing most of the screening. Additional screening compound(s) soluble in aqueous methanol with an absorption maximum at 335 nm played a minor role. Thus, cells are protected against potentially high levels of UV radiation by the snow itself when they live several centimeters beneath the surface, and they rely on cellular screening compounds, chiefly astaxanthin, when located near the surface where UV fluxes are high.

INTRODUCTION

Snow tinged with red color is a common and often conspicuous feature of the summer alpine environment. Colored snow arouses the curiosity of casual observers and scientists alike. Different algae living in the snow may color it yellow, green, orange, gray or red. Red snow caused by Chlamydomonas nivalis (Bauer) Wille and colloquially termed "watermelon snow" is most common. The spherical cells of this green alga are 10-50 [mu]m in diameter, and their centrally located nucleus and chloroplast are surrounded by lipid droplets filled with the secondary carotenoid astaxanthin and its esters with fatty acids (1-3). This is the same pigment that gives salmon and shrimp their distinctive pink hue.

C. nivalis is found worldwide, generally blooming in snow above 2500 m where snowfields persist into the summer (4-13). This environment, with cold temperatures and high irradiance, is especially harsh for a photosynthetic organism. In higher plants, these conditions normally cause severe photoinhibition because the cold temperatures slow the biochemical reactions of carbon fixation more than the light reactions. As a result of this imbalance, the absorbed light energy can cause photooxidation instead of being used in the Calvin cycle. The photosynthetically active radiation (PAR) in the alga's snowy environment can be very high (14). PAR can be high in the mountains, and reflection by snow can nearly double the exposure of algal cells at the snow surface, giving photon fluence rates approaching 5000 [mu]mol m^sup -2^ s^sup -1^. With increasing snow depth, light becomes isotropic and PAR drops exponentially so that cells growing deeper within the snow are exposed to less potentially damaging levels of light. On the other hand, the snow melts rapidly during the summer months and cells are moved by meltwater so that their location within the vertical profile of the snowpack can change dynamically throughout the day (15).

Despite their harsh environment, these cells are photosynthetically active (4,16-19), and they have mechanisms to protect them from photoinhibition. For example, the alga's red color, caused by astaxanthin, is central to its ability to withstand high levels of PAR (2,3,20,21). The astaxanthin screens out all but a small part of the incident blue light before it reaches the chloroplasts and thus reduces the amount of light available to the photosystems by about 50% (14). Screening is thus a first line of defense against the potentially high PAR fluence rates within the snow.

The alga's environment includes high levels of ultraviolet (UV) as well as visible (VIS) radiation, and its ability to withstand the UV is less well understood. The amount of UV radiation increases dramatically with altitude; so above 3000 m, UV irradiance can be 30% greater than at sea level (22). This altitude effect is wavelength-dependent, and it is more pronounced for UV radiation of wavelengths 280-315 nm (UV-B) than for UV radiation of wavelengths 315-400 nm (UV-A) (23). UV can cause many types of cellular damage, including damage to DNA and membranes, as well as photoinhibition of photosynthesis. Although photosystem I can be damaged by UV-B, photosystem II (PSII) appears to be the main target within the photosynthetic machinery, and as with photodamage by VIS light, the D1 protein in the reaction center is degraded (24). In addition, UV-B can influence carbon reduction through effects on both the quantity (25) and activity (26) of rubisco.

We focus our investigation on two questions concerning C. nivalis and its UV environment. First, we characterize the UV environment of C. nivalis in situ in the snow to determine the actual UV exposure. Second, we investigate screening as a mechanism for protection against the potentially harmful UV radiation, exploring whether screening compounds might be localized in the cell walls, cytoplasm or both.