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. Overall design: Samples from three independent cultures were withdrawn.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