Synechococcus picocyanobacteria are ubiquitous and abundant photosynthetic organisms in the marine environment and contribute for an estimated 16% of the ocean net primary productivity. Their light-harvesting complexes, called phycobilisomes (PBS), are composed of a conserved allophycocyanin core from which radiates six to eight rods with variable phycobiliprotein and chromophore content. This variability allows Synechococcus to optimally exploit the wide variety of spectral niches existing in marine ecosystems. Seven distinct pigment types or subtypes have been identified so far in this taxon, based on the phycobiliprotein composition and/or the proportion of the different chromophores in PBS rods. Most genes involved in their biosynthesis and regulation are located in a dedicated genomic region called the PBS rod region. Here, we examined the variability of gene sequences and organization of this genomic region in a large set of sequenced isolates and natural populations of Synechococcus representative of all known pigment types. All regions start with a tRNA-PheGAA and some possess mobile elements including tyrosine recombinases, suggesting that their genomic plasticity relies on a tycheposon-like mechanism. Comparison of the phylogenies obtained for PBS and core genes revealed that the evolutionary history of PBS rod genes differs from the rest of the genome and is characterized by the co-existence of different alleles and frequent allelic exchange. We propose a scenario for the evolution of the different pigment types and highlight the importance of population-scale mechanisms in maintaining a wide diversity of pigment types in different Synechococcus lineages despite multiple speciation events.

Biodiversity has always been predominantly microbial and the scarcity of fossils from bacteria, archaea and microbial eukaryotes has prevented a comprehensive dating of the tree of life. Here we show that patterns of lateral gene transfer deduced from the analysis of modern genomes encode a novel and abundant source of information about the temporal coexistence of lineages throughout the history of life. We use new phylogenetic methods to reconstruct the history of thousands of gene families and demonstrate that dates implied by gene transfers are consistent with estimates from relaxed molecular clocks in Bacteria, Archaea and Eukaryotes. An inspection of discrepancies between transfers and clocks and a comparison with mammal fossils show that gene transfer in microbes is potentially as informative for dating the tree of life as the geological record in macroorganisms.Until Zuckerkandl and Pauling put forth the "molecular clock" 1 hypothesis, the geological record alone provided the timescale for evolutionary history. Their demonstration that distances between amino acid sequences correlate with divergence times estimated from fossils demonstrated that information in DNA can be used to date the Tree of Life. Since then, the theory and methodology of the molecular clock have been developed extensively, and inferences from clock analyses (such as the diversification of placentals before the demise of dinosaurs 2,3 ) hotly debated. Despite these controversies, combining information from rocks and clocks is now widely accepted to be indispensable 3,4,5 : state-of-the-art estimates of divergence times rely on sequence based relaxed molecular clocks anchored by multiple fossil calibrations. This approach provides information on both the absolute timescale and the relative variation of the evolutionary rates across the phylogeny (Fig.1a). Yet, because most life is microbial, and most microbes do not fossilize, major uncertainties remain about the ages of microbial groups and the timing of some of the earliest and most important events in life's evolutionary history 6,7 .In addition to leaving only a faint trail in the geological record, the evolution of microbial life has also left a tangled phylogenetic signal due to extensive lateral gene transfer (LGT).LGT, the acquisition of genetic material potentially from distant relatives, has long been considered an obstacle for reconstructing the history of life 8 , because different genetic markers can yield conflicting estimates of the species phylogeny. However, it has been previously shown that transfers identified using appropriate phylogenetic methods carry information that can be harnessed to reconstruct species history 9-14 . This is possible because different hypotheses of species relationships yield different LGT scenarios and can thus be evaluated using phylogenetic models of genome evolution [15][16][17][18][19] . But in addition to carrying information about the relationships among species, transfers should also carry a record of the timing of species diversificat...