Phototrophic pigment diversity and picophytoplankton in permafrost thaw lakes

Abstract

Permafrost thaw lakes (thermokarst lakes) are widely distributed across the northern landscape, and are known to be biogeochemically active sites that emit large amounts of carbon to the atmosphere as CH4 and CO2. However, the abundance and composition of the photosynthetic communities that fix CO2 have been little explored in this ecosystem type. In order to identify the major groups of phototrophic organisms and their controlling variables, we sampled 12 permafrost thaw lakes along a permafrost degradation gradient in northern Québec, Canada. Additional samples were taken from five rock-basin reference lakes in the region to determine if the thaw lakes differed in limnological properties and phototrophs. Phytoplankton community structure was determined by high-performance liquid chromatography analysis of their photoprotective and photosynthetic pigments, and autotrophic picoplankton concentrations were assessed by flow cytometry. One of the black-colored lakes located in a landscape of rapidly degrading palsas (permafrost mounds) was selected for high-throughput 18S rRNA sequencing to complement conclusions based on the pigment and cytometry analyses. The results showed that the limnological properties of the thaw lakes differed significantly from the reference lakes, and were more highly stratified. However, both waterbody types contained similarly diverse phytoplankton groups, with dominance of the pigment assemblages by fucoxanthin-containing taxa, as well as chlorophytes, cryptophytes and cyanobacteria. Chlorophyll a concentrations (Chl a) were correlated with total phosphorus (TP), and both were significantly higher in the thaw lakes (overall means of 3.3 µg Chl a L−1 and 34 µg TP L−1) relative to the reference lakes (2.0 µg Chl a L−1 and 8.2 µg TP L−1). Stepwise multiple regression of Chl a against the other algal pigments showed that it was largely a function of alloxanthin, fucoxanthin and Chl b (R2 = 0.85). The bottom waters of two of the thaw lakes also contained high concentrations of bacteriochlorophyll d, showing the presence of green photosynthetic sulphur bacteria. The molecular analyses indicated a relatively minor contribution of diatoms, while chrysophytes, dinoflagellates and chlorophytes were well represented; the heterotrophic eukaryote fraction was dominated by numerous ciliate taxa, and also included Heliozoa, Rhizaria, chytrids and flagellates. Autotrophic picoplankton occurred in biovolume concentrations up to 3.1 × 105 µm3 picocyanobacteria mL−1 and 1.9 × 106 µm3 picoeukaryotes mL−1, with large variations among lakes. Both groups of picophytoplankton were positively correlated with total phytoplankton abundance, as measured by Chl a; picocyanobacteria were inversely correlated with dissolved organic carbon, while picoeukaryotes were inversely correlated with conductivity. Despite their net heterotrophic character, subarctic thaw lakes are rich habitats for diverse phototrophic communities.