Ruben Sommaruga

The role of solar UV radiation in the ecology of alpine lakes

Solar ultraviolet radiation (UVR, 290-400 nm) is a crucial environmental factor in alpine lakes because of the natural increase of the UVR flux with elevation and the high water transparency of these ecosystems. The ecological importance of UVR, however, has only recently been recognized. This review, examines the general features of alpine lakes regarding UVR, summarizes what is known about the role of solar UVR in the ecology of alpine lakes, and identifies future research directions. Unlike the pattern observed in most lowland lakes, variability of UV attenuation in alpine lakes is poorly explained by differences in dissolved organic carbon (DOC) concentrations, and depends mainly on optical characteristics (absorption) of the chromophoric dissolved organic matter (CDOM). Within the water column of lakes with low DOC concentrations (0.2-0.4 mg l(-1)), UV attenuation is influenced by phytoplankton whose development at depth (i.e. the deep chlorophyll maximum) causes important changes in UV attenuation. Alpine aquatic organisms have developed a number of strategies to minimize UV damage. The widespread synthesis or bioaccumulation of different compounds that directly or indirectly absorb UV energy is one such strategy. Although most benthic and planktonic primary producers and crustacean zooplankton are well adapted to high intensities of solar radiation, heterotrophic protists, bacteria, and viruses seem to be particularly sensitive to UVR. Understanding the overall impact of UVR on alpine lakes would need to consider synergistic and antagonistic processes resulting from the pronounced climatic warming, which have the potential to modify the UV underwater climate and consequently the stress on aquatic organisms.

Abundances, Identity, and Growth State of Actinobacteria in Mountain Lakes of Different UV Transparency

ABSTRACT The occurrence, identity, and activity of microbes from the class Actinobacteria was studied in the surface waters of 10 oligo- to mesotrophic mountain lakes located between 913 m and 2,799 m above sea level. Oligonucleotide probes were designed to distinguish between individual lineages within this group by means of fluorescence in situ hybridization (FISH). Bacteria of a single phylogenetic lineage (acI) represented >90% of all Actinobacteria in the studied lakes, and they constituted up to 70% of the total bacterial abundances. In the subset of eight lakes situated above the treeline, the community contribution of bacteria from the acI lineage was significantly correlated with the ambient levels of solar UV radiation (UV transparency, r2 = 0.72; P < 0.01). Three distinct genotypic subpopulations were distinguished within acI that constituted varying fractions of all Actinobacteria in the different lakes. The abundance of growing actinobacterial cells was estimated by FISH and immunocytochemical detection of bromodeoxyuridine (BrdU) incorporation into de novo-synthesized DNA. The percentages of Actinobacteria with visible DNA synthesis approximately corresponded to the average percentages of BrdU-positive cells in the total assemblages. Actinobacteria from different subclades of the acI lineage, therefore, constituted an important autochthonous element of the aquatic microbial communities in many of the studied lakes, potentially also due to their higher UV resistance.

Effect of Natural Sunlight on Bacterial Activity and Differential Sensitivity of Natural Bacterioplankton Groups in Northwestern Mediterranean Coastal Waters

ABSTRACT We studied the effects of natural sunlight on heterotrophic marine bacterioplankton in short-term experiments. We used a single-cell level approach involving flow cytometry combined with physiological probes and microautoradiography to determine sunlight effects on the activity and integrity of the cells. After 4 h of sunlight exposure, most bacterial cells maintained membrane integrity and viability as assessed by the simultaneous staining with propidium iodide and SYBR green I. In contrast, a significant inhibition of heterotrophic bacterial activity was detected, measured by 5-cyano-2,3 ditolyl tetrazolium chloride reduction and leucine incorporation. We applied microautoradiography combined with catalyzed reporter deposition-fluorescence in situ hybridization to test the sensitivity of the different bacterial groups naturally occurring in the Northwestern Mediterranean to sunlight. Members of the Gammaproteobacteria and Bacteroidetes groups appeared to be highly resistant to solar radiation, with small changes in activity after exposure. On the contrary, Alphaproteobacteria bacteria were more sensitive to radiation as measured by the cell-specific incorporation of labeled amino acids, leucine, and ATP. Within Alphaproteobacteria, bacteria belonging to the Roseobacter group showed higher resistance than members of the SAR11 cluster. The activity of Roseobacter was stimulated by exposure to photosynthetic available radiation compared to the dark treatment. Our results suggest that UV radiation can significantly affect the in situ single-cell activity of bacterioplankton and that naturally dominating phylogenetic bacterial groups have different sensitivity to natural levels of incident solar radiation.

Escape from UV threats in zooplankton : A cocktail of behavior and protective pigmentation

In order to avoid environmental threats, organisms may respond by altering behavior or phenotype. Using experiments performed in high-latitude Siberia and in temperate Sweden, we show for the first time that, among freshwater crustacean zooplankton, the defense against threats from ultraviolet radiation (UV) is a system where phenotypic plasticity and behavioral escape mechanisms function as complementary traits. Freshwater copepods relied mainly on accumulating protective pigments when exposed to UV radiation, but Daphnia showed strong behavioral responses. Pigment levels for both Daphnia and copepods were generally higher at higher latitudes, mirroring different UV threat levels. When released from the UV threat, Daphnia rapidly reduced (within 10 days) their UV protecting pigmentation-by as much as 40%--suggesting a cost in maintaining UV protective pigmentation. The evolutionary advantage of protective pigments is, likely, the ability to utilize the whole water column during daytime; conversely, since the amount of algal food is generally higher in surface waters, unpigmented individuals are restricted to a less preferred feeding habitat in deeper waters. Our main conclusion is that different zooplankton taxa, and similar taxa at different latitudes, use different mixes of behavior and pigments to respond to UV radiation.

Dust inputs and bacteria influence dissolved organic matter in clear alpine lakes.

Remote lakes are usually unaffected by direct human influence, yet they receive inputs of atmospheric pollutants, dust, and other aerosols, both inorganic and organic. In remote, alpine lakes, these atmospheric inputs may influence the pool of dissolved organic matter, a critical constituent for the biogeochemical functioning of aquatic ecosystems. Here, to assess this influence, we evaluate factors related to aerosol deposition, climate, catchment properties, and microbial constituents in a global dataset of 86 alpine and polar lakes. We show significant latitudinal trends in dissolved organic matter quantity and quality, and uncover new evidence that this geographic pattern is influenced by dust deposition, flux of incident ultraviolet radiation, and bacterial processing. Our results suggest that changes in land use and climate that result in increasing dust flux, ultraviolet radiation, and air temperature may act to shift the optical quality of dissolved organic matter in clear, alpine lakes.

Ultraviolet Radiation in a High Mountain Lake of the Austrian Alps: Air and Underwater Measurements

Global UV radiation was measured with a portable multichannel filter radiometer at the surface and underwater in a high mountain lake (2417 m above sea level) of the Austrian Alps during 16 days in summer 1995. During this period, total column ozone values that changed only by 34 Dobson units explained a significant part of the variability in UVB radiation at 305 nm as indicated by the negative correlation with the ratio 305:340 nm (rs= ‐0.810, P < 0.01). High radiation at the surface combined with high water transparency allowed substantial UVB radiation to reach the bottom of this lake. The diffuse attenuation coefficient for downward irradiance at 305 nm changed within 2 weeks from 0.24 m‐1 (10% at 9.6 m depth) to 0.32 m‐1 (10% at 7.2 m depth). This change in attenuation was related to the development of phytoplankton after the ice break‐up as indicated by a six‐fold increase in chlorophyll‐a concentrations during this period. Our results suggest that phytoplankton and/ or phytoplankton‐derived organic substances are important for the UV attenuation in this oligotrophic lake.

Differences in UV transparency and thermal structure between alpine and subalpine lakes: implications for organisms

Ultraviolet (UV) radiation is a globally important abiotic factor influencing ecosystem structure and function in multiple ways. While UV radiation can be damaging to most organisms, several factors act to reduce UV exposure of organisms in aquatic ecosystems, the most important of which is dissolved organic carbon (DOC). In alpine lakes, very low concentrations of DOC and a thinner atmosphere lead to unusually high UV exposure levels. These high UV levels combine with low temperatures to provide a fundamentally different vertical structure to alpine lake ecosystems in comparison to most lowland lakes. Here, we discuss the importance of water temperature and UV transparency in structuring alpine lake ecosystems and the consequences for aquatic organisms that inhabit them. We present transparency data on a global data set of alpine lakes and nearby analogous subalpine lakes for comparison. We also present seasonal transparency data on a suite of alpine and subalpine lakes that demonstrate important differences in UV and photosynthetically active radiation (PAR, 400-700 nm) transparency patterns even within a single region. These data are used to explore factors regulating transparency in alpine lakes, to discuss implications of future environmental change on the structure and function of alpine lakes, and ways in which the UV transparency of these lakes can be used as a sentinel of environmental change.

Blooms of single bacterial species in a coastal lagoon of the southwestern Atlantic Ocean.

ABSTRACT We investigated seasonal differences in community structure and activity (leucine incorporation) of the planktonic bacterial assemblage in the freshwater and brackish-water zones of a shallow coastal lagoon of the southwestern Atlantic Ocean. Alphaproteobacteria formed the dominant microbial group in both zones throughout the sampling period. After an intrusion of marine water, members of the SAR11 lineage became abundant in the brackish-water zone. These bacteria were apparently distributed over the lagoon during the following months until they constituted almost 30% of all prokaryotic cells at both sampling sites. At the first sampling date (March 2003) a single alphaproteobacterial species unrelated to SAR11, Sphingomonas echinoides, dominated the microbial assemblages in both zones of the lagoon concomitantly with a bloom of filamentous cyanobacteria. Pronounced maxima of leucine incorporation were observed once in each zone of the lagoon. In the freshwater zone, this highly active microbial assemblage was a mix of the typical bacteria lineages expected in aquatic systems. By contrast, a single bacterial genotype with >99% similarity to the facultative pathogen gammaproteobacterial species Stenotrophomonas maltophilia formed >90% of the bacterial assemblage (>107 cell ml−1) in the brackish-water zone at the time point of highest bacterial leucine incorporation. Moreover, these bacteria were equally dominant, albeit less active, in the freshwater zone. Thus, the pelagic zone of the studied lagoon harbored repeated short-term blooms of single bacterial species. This finding may have consequences for environmental protection.

Differential Sunlight Sensitivity of Picophytoplankton from Surface Mediterranean Coastal Waters

ABSTRACT We tested the sensitivity of coastal picophytoplankton exposed to natural sunlight in short-term experiments. Cell abundance and cell-specific chlorophyll fluorescence were significantly reduced in Prochlorococcus spp. but not in Synechococcus, whereas picoeukaryotes had an intermediate response. These results are the first direct evidence of a differential sensitivity to sunlight of these ubiquitous marine members of unicellular phytoplankton.

Constitutive and UV-inducible synthesis of photoprotective compounds (carotenoids and mycosporines) by freshwater yeasts

Twelve yeasts isolated from lakes of Northwestern Patagonia, Argentina, belonging to eight genera (Sporobolomyces, Sporidiobolus, Rhodotorula, Rhodosporidium, Cystofilobasidium, Cryptococcus, Torulaspora, and Candida) were analysed for their ability to produce photoprotective compounds. For this purpose, three laboratory experiments were performed to study the effect of photosynthetically active radiation (PAR) and PAR in combination with UV radiation (PAR + UVR) on the production of carotenoids and mycosporines. The synthesis of carotenoid compounds was clearly stimulated in six out of nine red yeast strains tested upon exposure to PAR or PAR + UVR; however, the latter conditions produced a stronger response than PAR alone. The increase in carotenoids in the red strains under PAR + UVR irradiation showed a negative exponential relationship with their basal carotenoid content, suggesting that cells with higher constitutive levels of carotenoids are less responsive to induction by PAR + UVR. Three red yeasts, Rhodotorula minuta, Rh. pinicola, and Rhodotorula sp., and the colourless Cryptococcus laurentii produced a UV-absorbing compound when exposed to PAR or PAR + UVR. This compound showed an absorption maximum at 309-310 nm and was identified as mycosporine-glutaminol-glucoside (myc-glu-glu). In these strains, exposure to PAR or PAR + UVR resulted in elevated concentrations of both carotenoids and myc-glu-glu. This is the first report on the production of mycosporines by yeasts. All strains that developed under PAR + UVR were able to synthesise carotenoids either constitutively or in response to PAR exposure, and a few of them also produced myc-glu-glu when exposed to PAR. Collectively, our results suggest that the presence of carotenoids, either alone or in combination with mycosporines, are required for sustaining growth under exposure to PAR + UVR in the freshwater yeast strains studied.