Evolution in action: habitat transition from sediment to the pelagial leads to genome streamlining in Methylophilaceae
Freshwater lakes are numerically dominated by very small microbes that appear perfectly adapted to nutrient poor (oligotrophic) conditions because of efficient resource exploitation in nM concentrations. The genomes of such oligotrophs are characterized by being very small (streamlined, <1.5 Mbp) with highly conserved core genomes and few pseudogenes, high coding densities, reduced numbers of paralogs, and a low genomic GC content. While genetic drift has been proposed as the evolutionary mechanism behind the reduced genomes of symbionts, parasites and commensals, selection driven by environmental factors seems to be the primary driving force for abundant free-living microbes.
Yet the evolutionary path of streamlining remains largely unknown because of obstacles in establishing axenic cultures of such oligotrophic microbes. We have developed an isolation strategy for oligotrophic freshwater microbes based on targeted enrichment and high-throughput dilution-to-extinction cultivation. Our current GACR project (19-23469S) focuses on a group of methylotrophic freshwater microbes (‘Ca. Methylopumilus’, Methylophilaceae) that are highly abundant in lakes and have very small cell and genome sizes (1.3 Mbp genome size).
In this study, we sequenced the complete genomes of 39 strains of ‘Ca. Methylopumilus’ as well as several other members of the family isolated from Řimov reservoir (Czechia) and Lake Zurich (Switzerland). Phylogenomic analyses resulted in the proposal of several novel taxa, i.e. ‘Ca. Methylopumilus rimovensis’ (strains from Řimov reservoir), ‘Ca. Methylopumilus universalis’ (strains from Lake Zurich and Řimov reservoir), ‘Ca. Methylosemipumilus turicensis’ (one strain from Lake Zurich).
The closest relatives of ‘Ca. Methylopumilus’ inhabit lake sediments and the pelagial of oceans, and we proposed that the evolutionary origin of the family can be traced back to sediment microbes with medium-sized genomes. The series of steps in the evolution of these genome-streamlined microbes was reconstructed via comparative genomics including all publicly available genomes of the family Methylophilaceae. A broad genomic spectrum is visible in the family Methylophilaceae, from freshwater sediment microbes with medium-sized genomes (Methylotenera, Methylophilus, 2–3 Mbp genome size), an occasionally blooming pelagic intermediate (‘Ca. Methylosemipumilus turicensis’, 1.7 Mbp), and the most reduced pelagic forms (‘Ca. Methylopumilus’ and marine OM43, 1.3 Mbp). We could show that a habitat transition from freshwater sediment to the relatively oligotrophic pelagial was accompanied by progressive gene loss and adaptive gains. Gene loss has mainly affected functions not necessarily required or advantageous in the pelagial or is encoded by redundant pathways. Likewise, we identified genes providing adaptations to oligotrophic conditions that have been transmitted horizontally from pelagic freshwater microbes (e.g., rhodopsins). Remarkably, the secondary transition from the pelagial of lakes to the oceans was not accompanied by further genome reduction, but by genome remodeling, i.e., adaptations to higher salinity, gained via horizontal gene transfer from indigenous microbes.
Figure: Phylogenomic tree based on 878 common concatenated proteins (351,312 amino acid sites) with Methyloversatilis sp. RAC08 as outgroup. Isolation sources or main habitats of strains are indicated by different colors, genome sizes are shown with circles of proportional size and GC content is depicted within each circle.
Our study provides first genomic evidence of genome reduction taking place during habitat transitions. In this regard, the family Methylophilaceae is an exceptional model for tracing the evolutionary history of genome streamlining as such a collection of evolutionarily related microbes from different habitats is rare in the microbial world.
The full text of the paper is available in The ISME Journal.