An Aerobic Anoxygenic Phototrophic Bacterium Fixes CO2 via the Calvin-Benson-Bassham Cycle

Aerobic anoxygenic phototrophic bacteria (AAnPB) are presently known as photoheterotrophs, which use light as auxiliary energy and whose growth is dependent on organic carbon (OC). But herein, we reported an unusual AAnPB strain of B3. True AAnPB is this strain because its growth requirement for oxygen and the harbouring specific genes cbb3- and bd-type cytochrome and acsF, and the production of bacteriochlorophyll in AAnPB. The genome showed this isolate had the complete metabolic pathways for the light utilization of AAnPB, CO2 fixation via Calvin-Benson-Bassham (CBB) cycle and the oxidation for sulfate and H2, and the transcriptome indicated that all components of these pathways were fully transcribed. The expression levels of the marker genes related to photosynthesis, including pufM for light harnessing and rbcL for CO2 fixation, and the activity of RubisCo, the key enzyme in the Calvin-Benson-Bassham (CBB) cycle, increased in response to decreased OC supply. Large amounts of cell biomass were obtained in liquid BG11 media under illumination. These suggested that the strain could photoautotrophically grow using sulfate or H2 as potential electron donors. That similar GC contents between the genes of photosynthetic gene clusters, CBB cycle and 16S rRNA, and the consistence of their phylogenetic topologies implied that light harnessing and carbon fixation genes evolved vertically from an anaerobic phototrophic ancestor of Rhodospirillaceae in alphaproteobacteria. In conclusion, strain B3 represents a novel AAnPB characterized by photoautotrophy using the CBB cycle. This kind of AAnPB may be ecologically significant in the global carbon cycle.