Research - Michaela Salcher's group

Eco-genomics of freshwater microbes

The major focus of our research is ecological niche partitioning of sympatric freshwater microbes with streamlined genomes. Freshwater microbes are centrally involved in chemical turnover processes, yet individual microbial populations and genotypes greatly differ in their respective metabolic and ecological features. We aim to get a synoptic view of the functional roles and phylogeographic distribution patterns of different microbial taxa and genotypes to identify the main drivers for their success in lakes.

The most abundant microbes in freshwater systems are of conspicuously small size (cell volumes <0.1 μm3) and have streamlined genomes (<1.5 Mb). Streamlining theory predicts that gene loss is caused by evolutionary selection driven by environmental factors, making these organisms superior competitors for limiting resources under oligotrophic conditions. Ecotype diversification reflects a possible niche-specific adaptation of closely related genotypes and a high degree of microdiversification might be the reason for the observed high total population numbers. Although such streamlined microbes numerically dominate in lakes, they are still poorly studied. Potential auxotrophies and dependencies on co-occurring organisms so far often prevent the establishment of axenic cultures, which, in turn has hampered an in-depth ecological assessment of the reasons for their success in nature. A newly developed isolation strategy for oligotrophs allowed us to bring some of these microbes temporarily in culture, e.g., members of the most abundant freshwater microbes, the acI Actinobacteria (newly proposed order Ca. Nanopelagicales’). Whole genome sequencing and comparative genomics in combination with high-resolution monitoring of distinct genotypes is applied for identifying microdiversification patterns in ubiquitous freshwater oligotrophs (Fig. 1). We aim to disentangle the underlying ecological reasons for the widespread but yet enigmatic phenomenon of genome-streamlining in freshwater microbes.

 

Salcher_Figure_1
Fig. 1: Whole-genome alignment of 11 ‘Ca. Planktophila’ strains. The genomes have been linearized for simplicity. Synteny and different degrees of sequence similarity are indicated by vertical lines connecting the genomes. rRNA operons in the individual genomes are displayed as red arrows and tRNAs as short vertical lines. Genomic islands (GI) have been marked in different colours and numbered. Red: genes encoding mainly cell wall biosynthesis and modifications; Green: genes encoding pilus assembly; Yellow: genes encoding mainly membrane transport and / or carbohydrate metabolism; Brown: unknown function.

Population-genomics of streamlined freshwater methylotrophs

We have a unique collection of strains (>150) with highly reduced genomes that were mainly isolated from the pelagial of Lake Zurich: Ca. Methylopumilus planktonicus’ (Methylophilaceae, Betaproteobacteria) are small, abundant planktonic methylotrophs with streamlined genomes (1.3 Mb). These strains are ideal models for comparative population-genomics of oligotrophic, highly specialized ultramicrobacteria with streamlined genomes. Preliminary data from 31 genome sequenced strains suggests a high degree of microdiversification with a large core genome and an unsaturated, highly flexible pan-genome. This ecotype diversification indicates possible niche-specific adaptations of closely related genotypes (>99.9% 16S rRNA similarity) and might explain high total population numbers.  

Ca. M. planktonicus’ serve also as perfect model organisms for studying adaptations to novel environments and the evolution of genome-streamlining per se. Their closest relatives inhabit the sediment of lakes and the pelagial of oceans (Fig. 2), and we propose that the evolutionary origin of the family can be traced back to sediment microbes with medium-sized genomes. Microbes affiliated with another planktonic methylotroph, ‘Ca. M. turicensis’, seem to be transitional taxa that crossed the border to the pelagial very recently. In this regard, the family Methylophilaceae is an exceptional model for tracing the evolutionary history of genome-streamlining as such a collection of evolutionary related microbes from different habitats is practically unknown for other important genome-streamlined microbes (e.g., ‘Ca. Pelagibacter’, ‘Ca. Nanopelagicales’).

Salcher_Figure_2
Fig. 2: Phylogenomic tree (450 concatenated conserved proteins) of the family Methylophilaceae. Genome sizes and GC content are displayed as symbols; freshwater ‘Ca. Methylopumilus spp.’ strains are highlighted in bold.

Moreover, most streamlined microbes possess light driven proton pumps (rhodopsins) that might help them to survive under oligotrophic conditions. However, the environmental conditions leading to an expression of these genes and the metabolic benefits of rhodopsins are still poorly understood. ‘Ca. M. planktonicus’ encode genes for 2 different types of rhodopsins (proteo- and xanthorhodopsins), while their closest relatives possess only one type or no rhodopsins at all. We aim to combine comparative genomics and experimental approaches to identify the ecological benefits of this photoheterotrophic lifestyle.