Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae

• Published in: The ISME Journal Vol. 12; no. 8; pp. 1994 - 2010
• Main Authors: Brinkmann, Henner, Göker, Markus, Koblížek, Michal, Wagner-Döbler, Irene, Petersen, Jörn
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.08.2018; Oxford University Press
• Subjects: 631/158/855; 631/181/757; 631/326/171/1878; Biological evolution; Biomedical and Life Sciences; Current distribution; Diagnostic systems; Ecology; Evolution; Evolutionary Biology; Gene transfer; Genes; Genomes; Horizontal transfer; Life Sciences; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Photosynthesis; Phototrophy; Phylogeny; Plasmids
• ISSN: 1751-7362; 1751-7370; 1751-7370
• DOI: 10.1038/s41396-018-0150-9

The capacity for anoxygenic photosynthesis is scattered throughout the phylogeny of the Proteobacteria . Their photosynthesis genes are typically located in a so-called photosynthesis gene cluster (PGC). It is unclear (i) whether phototrophy is an ancestral trait that was frequently lost or (ii) whether it was acquired later by horizontal gene transfer. We investigated the evolution of phototrophy in 105 genome-sequenced Rhodobacteraceae and provide the first unequivocal evidence for the horizontal transfer of the PGC. The 33 concatenated core genes of the PGC formed a robust phylogenetic tree and the comparison with single-gene trees demonstrated the dominance of joint evolution. The PGC tree is, however, largely incongruent with the species tree and at least seven transfers of the PGC are required to reconcile both phylogenies. The origin of a derived branch containing the PGC of the model organism Rhodobacter capsulatus correlates with a diagnostic gene replacement of pufC by pufX . The PGC is located on plasmids in six of the analyzed genomes and its DnaA-like replication module was discovered at a conserved central position of the PGC. A scenario of plasmid-borne horizontal transfer of the PGC and its reintegration into the chromosome could explain the current distribution of phototrophy in Rhodobacteraceae .