Research

Bacteria are found everywhere: in clouds and raindrops, on tree leaves, in soil and oceans, on and in our body. Unlike eukaryotes, bacterial evolution comprises both vertical and horizontal components. Recombination at the species level plays a role in selective sweeps through the population, while inter-species lateral gene transfer (LGT) has important implications to microbial adaptation and evolutionary transformations. In our research we study molecular and genome evolution of microbial genomes.


The extent of lateral gene transfer during microbial evolution

Lateralgenetransfer
(Popa and Dagan 2011)

To quantify the extent of LGT in microbial genomes, we apply phylogenomic network approaches that we developed (Dagan 2011). For example, studying genome evolution in cyanobacteria, our networks approach revealed that 60% of cyanobacterial gene families have been affected by LGT (Dagan et al. 2013). Our networks approach can be applied also to specific gene transfer mechanisms. The analysis of phage-mediated LGTs using directed networks revealed that most transduction events are between closely related donors and recipient. This implies that host-specificity constitutes a barrier for LGT by phages {Popa:2016gq}. In our research of genome evolution by lateral gene transfer we also touch upon evolution by gene transfer in eukaryotes. In one study we presented an evolutionary link between the plastid acquisition event and the evolution of redox sensitive proteins by endosymbiotic gene transfer (Woehle et al. 2017). In another study we discovered that the denitrification pathway in foraminifera (unicellular eukaryotes) is of prokaryotic origins, hence the evolution of denitrification in foraminifera constitutes a rare example for an acquisition of prokaryotic genes in eukaryotes (Woehle et al. 2018).

Evolution of autonomously replicating genetic elements – phages and plasmids

Plasmid life cycles
(Hülter et al. 2017)

Plasmids and phages are genetic elements that colonize and replicate in prokaryotic cells. They are considered a major driving force of prokaryote evolution as they can migrate between cells and populations, making them potent agents of lateral DNA transfer. The evolution of phages themselves includes DNA acquisition by lateral transfer, and we recently quantified its magnitude in a study of genome evolution in dairy phages. In that study we also showed that the rate of recombination is constant and is 24-fold higher than the rate of mutation (Kupczok et al. 2018). A special focus in our group is the evolution of plasmid genomes (Hülter et al. 2017). Our study of genome evolution of multicopy plasmids presents evidence that plasmids evolve slower than chromosomes, due to the impact of segregational drift (Ilhan et al. 2018). This is a conceptually novel view on the evolution of plasmids and our current research is focused on characterizing that phenomenon.  

Evolution of multicellularity in cyanobacteria

Cyanobacteria phenotypes

(Koch et al. 2017)

Cyanobacteria perform oxygenic photosynthesis as their main energy source. They shaped Earth's history through the production of atmospheric oxygen starting >2.3 Gyr ago. Filamentous cyanobacteria that differentiate multiple cell types are considered the peak of prokaryotic complexity and their evolution has been studied in the context of multicellularity origins. In our research we are interested to reconstruct the order of events in the evolution of multicellular cyanobacteria. An important aspect of evolutionary inference is the interpretation of phylogenetic tree topology, and specifically, the inference of ancestor-descendant relations. For that purpose, we developed a phylogenetic rooting method using Minimal Ancestor Deviation (MAD) (Tria et al. 2017). The application of MAD to cyanobacteria genomes showed that the common ancestor of that group was a unicellular cyanobacterium; hence, multicellularity is a late development in that group. Our study of branching phenotypes further highlights the role of genetic assimilation in the evolution of colony morphology (Koch et al. 2017).
 

References

Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, Gould SB, Goremykin VV, Rippka R, Tandeau de Marsac N, et al. 2013. Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol. Evol. 5:31–44.

Dagan T. 2011. Phylogenomic networks. Trends Microbiol. 19:483–491.

Hülter N, Ilhan J, Wein T, Kadibalban AS, Hammerschmidt K, Dagan T. 2017. An evolutionary perspective on plasmid lifestyle modes. Curr. Opin. Microbiol. 38:74–80.

Ilhan J, Kupczok A, Woehle C, Wein T, Hülter NF, Rosenstiel P, Landan G, Mizrahi I, Dagan T. 2018. Segregational drift and the interplay between plasmid copy number and evolvability. Mol. Biol. Evol.

Koch R, Kupczok A, Stucken K, Ilhan J, Hammerschmidt K, Dagan T. 2017. Plasticity first: molecular signatures of a complex morphological trait in filamentous cyanobacteria. BMC Evolutionary Biology 17:209.

Kupczok A, Neve H, Huang KD, Hoeppner MP, Heller KJ, Franz CMAP, Dagan T. 2018. Rates of Mutation and Recombination in Siphoviridae Phage Genome Evolution over Three Decades. Mol. Biol. Evol. 35:1147–1159.

Popa O, Landan G, Dagan T. 2017. Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction. ISME J. 11:543–554.

Tria FDK, Landan G, Dagan T. 2017. Phylogenetic rooting using minimal ancestor deviation. Nat. Ecol. Evol. 1:193.

Woehle C, Dagan T, Landan G, Vardi A, Rosenwasser S. 2017. Expansion of the redox-sensitive proteome coincides with the plastid endosymbiosis. Nature Plants 3:17066.

Woehle C, Roy A-S, Glock N, Wein T, Weissenbach J, Rosenstiel P, Hiebenthal C, Michels J, Schönfeld J, Dagan T. 2018. A Novel Eukaryotic Denitrification Pathway in Foraminifera. Curr. Biol. 28:2536–2543.e5.