Characteristics and Evolutionary analysis of Photosynthetic Gene Clusters on Extrachromosomal Replicons: from streamlined plasmids to chromids

Abstract

AbstractAerobic anoxygenic photoheterotrophic bacteria (AAPB) represent intermediates in the evolution from photoautotrophic to heterotrophic metabolisms. Substantial evidence indicates that highly conserved photosynthetic gene clusters (PGCs) of AAPB can be transferred between species, genera, and even phyla. Furthermore, analysis of recently discovered PGCs carried by extrachromosomal replicons (exPGCs) suggests that extrachromosomal replicons (ECRs) play an important role in the transfer of PGCs. In the present study, thirteenRoseobacterclade genomes from seven genera that harbored exPGCs were used to analyze characteristics and evolution of PGCs. The identification of plasmid-like and chromid-like ECRs from PGC-containing ECRs revealed two different functions: the spread of PGCs among strains and the maintenance of PGCs within genomes. Phylogenetic analyses indicated two independent origins of exPGCs, corresponding to PufC-containing and PufX-containing photosynthetic reaction complexes. Furthermore, the two different types of complexes were observed within different strains of the sameTateyamariaandJannaschiagenera. The two different complexes were also differentially carried by chromosomes and ECRs in the strains, respectively, which provided clear evidence for ECR-mediated PGC transfer. Multiple recombination events of exPGCs were also observed, wherein the majority of exPGCs were inserted by replication modules at the same genomic positions. However, the exPGCs of theJannaschiastrains comprised superoperons without evidence of insertion, and therefore likely represent an initial evolutionary stage where the PGC was translocated from chromosomes to ECRs without further combinations. Lastly, a scenario of PGC gain and loss is proposed that specifically focuses on ECR-mediated exPGC transfer to explain the evolution and patchy distribution of AAPB within theRoseobacterclade.ImportanceThe evolution of photosynthesis was a significant event during the diversification of biological life. Aerobic anoxygenic heterotrophic bacteria (AAPB) share physiological characteristics with both photoautotrophs and heterotrophs and are therefore suggested to be evolutionary intermediates between the two lifestyles. Here, characterization and evolutionary analyses were conducted for thirteen bacterial strains that contained photosynthetic gene clusters (PGCs) carried by extrachromosomal replicons (ECRs) to shed light on the evolution of photosynthesis in bacteria. Specifically, these analyses improved the “Think Pink” scenario of PGC transfer that is mediated by ECRs inRoseobacterclade strains. This study advances our understanding of the importance of ECRs in the transfer of PGCs within marine photoheterotrophic bacteria.