Phototrophicity and genomic composition in plant-associated Sphingomonas faeni strains

Solar radiation impacts most life forms on Earth as an energy source or a regulatory signal. Still, relatively little is known about phototrophic potential and strategies of environmental bacteria beyond cyanobacteria. This study explores the phototrophy related genomic diversity of Sphingomonas faeni strains from boreal, sub-arctic and arctic regions. We analyzed the genomes of 25 plant-associated S. faeni strains isolated from Vaccinium myrtillus, Oxyria digyna, V. vitis-idaea, and Bistorta vivipara, along with a reference S. faeni genome MA-Olki. The strains showed diversity both in overall genome level but also in phototrophic capabilities: Seven strains were identified as aerobic anoxygenic phototrophic bacteria with a complete photosynthesis gene cluster, 16 strains contained xanthorhodopsin genes, and three strains were non-phototrophic, possessing no aerobic anoxygenic phototrophic or xanthorhodopsin genes. Aerobic anoxygenic phototrophic strains were found exclusively in Vaccinium hosts. O. digyna contained only xanthorhodopsin containing strains and B. vivipara showed xanthorhodopsin genes and one non-phototrophic strain. V. vitis-idaea hosted strains for all three different phototrophy categories. Phylogenetic analyses showed aerobic anoxygenic phototrophic positive strains forming a tight phylogenetic group. Xanthorhodopsin strains and non-phototrophic strains clustered into three different subgroups. Phototrophic strains had more photoreceptors. Aerobic anoxygenic phototrophic strains encoded two 5-aminolevulinic acid synthase isoenzymes, one from a hemT-like gene within the photosynthesis gene cluster and one from a hemA-like gene elsewhere in the genome. Our genomic analysis reveals substantial diversity in phototrophic potential among strains of a single bacterial species isolated from different host plants, possibly reflecting the distinct environmental cues each strain encountered.