Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)

Abstract

Marine picocyanobacteria, <i>Prochlorococcus</i> and <i>Synechococcus</i>, substantially contribute to marine primary production and have been the subject of extensive ecological and genomic studies. Little is known about their close relatives from freshwater and non-marine environments. Phylogenomic analyses (using 136 proteins) provide strong support for the monophyly of a clade of non-marine picocyanobacteria consisting of <i>Cyanobium, Synechococcus</i> and marine Sub-cluster 5.2; this clade itself is sister to marine <i>Synechococcus</i> and <i>Prochlorococcus</i>. The most basal lineage within the Syn/Pro clade, Sub-Cluster 5.3, includes marine and freshwater strains. Relaxed molecular clock (SSU, LSU) analyses show that while ancestors of the Syn/Pro clade date as far back as the end of the Pre-Cambrian, modern crown groups evolved during the Carboniferous and Triassic. Comparative genomic analyses reveal novel gene cluster arrangements involved in phycobilisome (PBS) metabolism in freshwater strains. Whilst PBS genes in marine <i>Synechococcus</i> are mostly found in one type of phycoerythrin (PE) rich gene cluster (Type III), strains from non-marine habitats, so far, appear to be more diverse both in terms of pigment content and gene arrangement, likely reflecting a wider range of habitats. Our phylogenetic analyses show that the PE genes (<i>mpeBA</i>) evolved via a duplication of the <i>cpeBA</i> genes in an ancestor of the marine and non-marine picocyanobacteria and of the symbiotic strains <i>Synechococcus spongiarum</i>. A 'primitive' Type III-like ancestor containing <i>cpeBA</i> and <i>mpeBA</i> had thus evolved prior to the divergence of the Syn/Pro clade and <i>S. spongiarum</i>. During the diversification of <i>Synechococcus</i> lineages, losses of <i>mpeBA</i> genes may explain the emergence of pigment cluster Types I, II, IIB, and III in both marine and non-marine habitats, with few lateral gene transfer events in specific taxa.