A Swiftian Voyage from Brobdingnag to Lilliput: Freshwater Planctomycetes drifting towards the poles of the genome size spectrum

Abstract

Freshwater environments teem with microbes. Currently, our apprehension of evolutionary ecology of freshwater bacteria is hampered by the difficulty to establish organism models for the most representative clades. To circumvent the bottlenecks inherent to the cultivation-based techniques, we applied ecogenomics approaches in order to unravel the evolutionary history and the processes that drive genome architecture in hallmark freshwater lineages from Planctomycetes phylum. The evolutionary history inferences showed that sediment/soil Planctomycetes transitioned to aquatic environments were, through processes mostly associated with reductive genome evolution, gave rise to new freshwater-specific clades. The most successful lineage was found to simultaneously have the most specialized lifestyle (increased regulatory genetic circuits; metabolism tuned for mineralization of proteinaceous sinking aggregates; psychrotrophic behavior) and to harbor the smallest genomes, highlighting a genomic architecture shaped by niche-directed evolution.