Final Report Summary - EVOLATERAL (The mechanisms for lateral gene transfer in nature as reflected in prokaryote genomes)
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. EVOLATERAL aimed to develop and use networks approaches for the research of microbial evolution by lateral gene transfer. Focusing on specific microbial taxa where we studied the impact of lateral gene transfer, for example, in halophilic archaea (Nelson-Sathi et al. 2012 doi: 10.1073/pnas.1209119109) where we detected hundreds of genes that were putatively transferred from eubacterial donors to the ancestor of haloarchaea. Our study suggested that LGT on a massive scale transformed a strictly anaerobic, chemolithoautotrophic methanogen into the heterotrophic, oxygen-respiring, and bacteriorhodopsin-photosynthetic haloarchaeal common ancestor. Focusing on genome evolution in cyanobacteria our networks approach revealed that 60% of cyanobacterial gene families have been affected by LGT (Dagan et al. 2013 doi: 10.1093/gbe/evs117). Working further on microbial evolution by LGT we then focused our attention on the impact of transduction (bacteriophage-mediate gene transfer) on LGT. Our 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 et al. 2017 doi: 10.1038/ismej.2016.116). 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, doi: 10.1093/molbev/msy027). Researching the impact of conjugation on LGT, we turned our attention to the evolution of the transfer vector itself – i.e. plasmids (Hülter et al. 2017 doi: 10.1016/j.mib.2017.05.001). 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 bioRxiv, 369579). This is a conceptually novel view on the evolution of plasmids and we expect that it will have a large impact on the field in the future. In our research of genome evolution by lateral gene transfer we also touched upon lateral gene transfer in eukaryotic evolution. In one study we presented an evolutionary link between the plastid acquisition event and the evolution of redox sensitive proteins by endosymbiotic gene transfer (Whöle et al. 2017 doi: 10.1038/nplants.2017.66). 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 (Whöle et al. 2018 doi: 10.1016/j.cub.2018.06.027). An important aspect of LGT inference is the interpretation of phylogenetic tree topology, and specifically, the inference of ancestor-descendant relations. Phylogenetic tree reconstruction methods produce unrooted trees, which require an additional analysis – rooting – in order to determine the ancestor-descendant relations of the studied entities. An important methodological development in EVOLATERAL is a novel rooting method using Minimal Ancestor Deviation (MAD), which operates on any phylogenetic tree with branch lengths (Tria et al. 2017 doi: 10.1038/s41559-017-0193). We anticipate that many long-standing evolutionary controversies will be settled with high-quality rooting. The application of MAD to cyanobacteria showed that the common ancestor of that group was most likely a marine cyanobacterium, hence we conclude that the basic photosynthetic machinery originated in a marine environment. In summary, EVOLATERAL contributed to the discovery of LGT events and the understanding of LGT impact on genome evolution.