Niche-directed evolution modulates genome architecture in freshwater Planctomycetes

Adrian-Ştefan Andrei,Petr Znachor,Michaela M Salcher,Pavel Rychtecký,Maliheh Mehrshad,Rohit Ghai

doi:10.1038/s41396-018-0332-5

Abstract

Freshwater environments teem with microbes that do not have counterparts in culture collections or genetic data available in genomic repositories. 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 the phylum Planctomycetes. The evolutionary history inferences showed that sediment/soil Planctomycetes transitioned to aquatic environments, where they gave rise to new freshwater-specific clades. The most abundant lineage was found to have the most specialised lifestyle (increased regulatory genetic circuits, metabolism tuned for mineralization of proteinaceous sinking aggregates, psychrotrophic behaviour) within the analysed clades and to harbour the smallest freshwater Planctomycetes genomes, highlighting a genomic architecture shaped by niche-directed evolution (through loss of functions and pathways not needed in the newly acquired freshwater niche).

Highlights

Planctomyces bacteria [1] encompass one of the most enigmatic branches of the prokaryotic tree of life that have been brought into axenic culture [2]
By making use of high spatial scale data we show that Planctomycetes are ubiquitously present in aquatic habitats and sediments, where their contribution to prokaryotic assemblages varies by environmental spatial heterogeneity and to a lesser extent, habitat (Fig. 1, Supplementary Figure 1)
The fluctuation in abundance, within prokaryotic community structure (e.g., Lake Zurich, samples collected on 13th of May 2013; Fig. 1), from scarcely present (0.1% rRNA gene reads in the epilimnion) to highly abundant (13.1% rRNA gene reads in the hypolimnion) pointed towards a niche, rather than habitat, preference

Summary

Introduction

Planctomyces bacteria (sensu Woese et al.) [1] encompass one of the most enigmatic branches of the prokaryotic tree of life that have been brought into axenic culture [2]. This division, envisioned as a phylum [3], was thought to accommodate members that either rooted deeply in the bacterial line of descent [4] or paved the way to eukaryality [5, 6].

Methods

Results

Conclusion