Psychrotolerant bacterium Sphingomonas glacialis AAP5 harvests light energy using both proton-pumping xanthorhodopsins and bacteriochlorophyll-based reaction centers

Bacterium Sphingomonas glacialis AAP5 isolated from the alpine lake Gossenköllesee contains genes for anoxygenic phototrophy as well as proton-pumping xanthorhodopsin. Here we show that AAP5 expresses xanthorhodopsin when illuminated at temperatures below 16°C. In contrast bacteriochlorophyll-containing reaction centers are expressed between 4 and 22°C in the dark. Thus, cells grown at lower temperature under natural light-dark cycle produced both photosystems. The purified xanthorhodopsin contains carotenoid nostoxanthin serving as an auxiliary antenna and performs the standard photocycle. The xanthorhodopsin-containing cells reduced upon illumination their respiration, increased their ATP synthesis and produced more biomass. This documents that the harvested light energy was utilized in the metabolism, which can represent a competitive advance under carbon-limiting conditions. The presence of Sphingomonas bacteria with dual phototrophy was verified in the metagenomes collected from lake Gossenköllesee. This unique trait may represent a metabolic advantage in alpine lakes where photoheterotrophic organisms facelimited organic substrates, low temperature, and extreme changes in irradiance. Samples from three independent cultures were withdrawn. Each of the three replicate cultures were sampled for three consenquent days. Each day, samples were taken 1 h and 6 h after the switch to light and 1 h and 6 h after the switch to dark phase of cultivation