Extensive recombination, selection, and asexual blooms shapethe diversity of the dominant clade of Prochlorococcus

Abstract

The tiny and enormously abundant marine cyanobacterium Prochlorococcus marinus contains many levels of population structure, with sequenced isolates spanning four orders of magnitude of diversity. It is divided into several major clades which exhibit the classic structure of distinct species, with little gene exchange across clade boundaries. The diversity within the dominant clade, High Light II (HLII), exceeds that of many bacterial species but exhibits little global population structure beyond some small tight genomic clusters. Few ecological distinctions within HLII have been found. What causes and sustains for millions of years the extensive diversity of this globally mixed population? In this work, hundreds of single cell genomes are analyzed and used to elucidate patterns of core and flexible gene flow, delineate subtle geographical correlations, and quantitatively test several scenarios for the evolutionary history of HLII. We find that recombination connects the entire HLII clade and that genes more than a few kb apart along the genome evolve largely independently. On shorter timescales, primarily-asexual blooms occur, but the clonal backbones of the resulting closely-related cell clusters are steadily eroded by recombination with the rest of HLII. Although a small number of genes have ocean-specific alleles, there is no evidence for genetically-stable ecotypes within the clade. We conjecture that spatio-temporally variable selection drives conditionally-beneficial variants of genomic segments to rise to high abundance while horizontally-transferring throughout the population.

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