Strain-Level Genetic Diversity of a Cyanobacterial Population

Advances in DNA sequencing have made it possible to sample metagenomes,amplicons, and multiple whole genomes from natural microbial populations, but it is amajor challenge to glean from such data the key evolutionary and ecological forcesthat have shaped a population. This challenge is sharpened when diverse members ofa single species are found to coexist. We studied the cyanobacterial Synechococcus sp.,a dominant member of the dense biofilms in the hot springs of Yellowstone NationalPark, focusing on the extensive diversity found within a single sample. We carried outdeep amplicon sequencing of many loci and analyzed multiple statistical properties ofthe data. We previously showed that the population has undergone an unexpectedlyhigh degree of homologous recombination, unlinking synonymous SNP-paircorrelations even on intragenic length scales. Here we investigate also the amino acidand genic-level diversity focusing on evidence of selection and hints to the evolutionaryhistory. Surprisingly, some features of the data, including the spectrum of distancesbetween the genic-alleles, appear consistent with primarily asexual neutral drift. Yet,the non-synonymous site frequency spectrum has too large an excess of low-frequencypolymorphisms to be purifying selection on deleterious mutations given thedistribution of coalescent times that we infer. And the population is not asexual.Taken all together, these seemingly contradictory data imply that selection, epistasis,and hitchhiking must be playing essential roles in creating and stabilizing the diversity.We discuss potential roles that ecological sub-division at the organismal or genic levelmay also play. From quantitative properties, including comparisons between two fullysequenced genomes and previous metagenome data, we infer aspects of the history andinter-spring dispersal of the meta-population since it was established in theYellowstone caldera. Our investigations illustrate the need for combining multipletypes of sequencing data and statistical analyses for developing understanding of subspecies-level diversity.