Abstract
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.
Highlights
Life on this planet originated in an anoxygenic environment and early microbial evolution was the age of anaerobes [1]
This would imply that the photosynthetic capacity entered Proteobacteria by horizontal gene transfer (HGT), a hypothesis that is in contrast to the earlier assumption that the ancestor of Proteobacteria performed anoxygenic PS and this ability was lost in some extant taxa [12,13,14]
Maximum likelihood (ML) trees were inferred from the supermatrices with ExaML v3.0.19 [29] using maximum-parsimony starting trees, automated detection of the best substitution model, and 100 bootstrap replicates to estimate the statistical support of the internal nodes
Summary
Life on this planet originated in an anoxygenic environment and early microbial evolution was the age of anaerobes [1]. Phototrophic Firmicutes (Heliobacteria), Chlorobi, and Acidobacteria utilize the iron sulfur-containing RC1 type, while Proteobacteria, Gemmatimonadetes, and Chloroflexi possess the RC2 that uses quinone electron acceptors [3]. Oxygenic cyanobacteria harbor both RC types that work in concert to bridge the large difference of the redox potential between water and NADP+. Based on comparative physiological analyses, it was suggested that anoxygenic PS originated in protocyanobacteria and later evolved into oxygenic PS [5] This would imply that the photosynthetic capacity entered Proteobacteria by HGT, a hypothesis that is in contrast to the earlier assumption that the ancestor of Proteobacteria performed anoxygenic PS and this ability was lost in some extant taxa [12,13,14]
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