Toward quantifying the adaptive role of bacterial pangenomes during environmental perturbations

Metagenomic surveys have revealed that natural microbial communities are predominantly composed of sequence-discrete, species-like populations but the genetic and/or ecological processes that maintain such populations remain speculative, limiting our understanding of population speciation and adaptation to perturbations. To address this knowledge gap, we sequenced 112 Salinibacter ruber isolates and 12 companion metagenomes from four adjacent saltern ponds in Mallorca, Spain that were experimentally manipulated to dramatically alter salinity and light intensity, the two major drivers of this ecosystem. Our analyses showed that the pangenome of the local Sal. ruber population is open and similar in size (~15,000 genes) to that of randomly sampled Escherichia coli genomes. While most of the accessory (noncore) genes were isolate-specific and showed low in situ abundances based on the metagenomes compared to the core genes, indicating that they were functionally unimportant and/or transient, 3.5% of them became abundant when salinity (but not light) conditions changed and encoded for functions related to osmoregulation. Nonetheless, the ecological advantage of these genes, while significant, was apparently not strong enough to purge diversity within the population. Collectively, our results provide an explanation for how this immense intrapopulation gene diversity is maintained, which has implications for the prokaryotic species concept.This work was partly funded by the US National Science Foundation, awards #1831582 and #1759831 (to KTK), and by the projects CLG2015_66686-C3-1-P, PGC2018-096956-B-C41, and RTC-2017-6405-1 of the Spanish Ministry of Science, Innovation and Universities (to RRM), which were also supported with European Regional Development Fund (FEDER) funds. RRM acknowledges the financial support of the sabbatical stay at Georgia Tech by the grant PRX18/00048 also from the Spanish Ministry of Science, Innovation and Universities