Contribution of Lateral Gene Transfer to the evolution of the eukaryotic fungus Piromyces sp. E2: Massive bacterial transfer of genes involved in carbohydrate metabolism

Abstract

ABSTRACTLateral gene transfer (also known as Horizontal Gene Transfer) is the transmission of genetic material between phylogenetically unrelated organisms. Previous studies have been showing the importance of this process for the evolution of unicellular eukaryotes, particularly those living in highly competitive niches such as the herbivore gut.Pyromices sp. is an obligate anaerobic chytrid fungus that grows as a commensal organism in the gut of mammalian herbivores, possessing hydrogenosomes instead of mitochondria, producing hydrogen, and playing a key role in the digestion of plant cell wall material. These particular features make its genome particularly valuable for the study of the evolution and adaptation of unicellular eukaryotes to the cellulose-rich and anaerobic environment of the herbivore gut.Here we performed a detailed large-scale lateral gene transfer (LGT) analysis of the genome from the chytrid fungus Piromyces sp. strain E2. For this we set out to elucidate (i) which proteins were likely transferred to its genome, (ii) from which bacterial donor species, and (iii) which functions were laterally acquired. Using sequence comparison and phylogenetic analyses, we have found 704 LGT candidates, representing nearly 5% of the Piromyces sp. orfeome (i.e. the complete set of open reading frames), mostly transferred from Firmicutes, Fibrobacteres, Bacteroidetes and Proteobacteria, closely following the microbial abundance reported for the herbivore gut. With respect to the functional analysis, the LGT candidate set includes proteins from 250 different orthologous groups, with a clear over-representation of genes belonging to the Carbohydrate Transport and Metabolism functional class. Finally, we performed a graph density analysis on the metabolic pathways formed by the LGT candidate proteins, showing that the acquired functions fit cohesively within Piromyces metabolic network, and are not randomly distributed within the global KEGG metabolic map. Overall, our study suggests that Piromyces’ adaptation to living anaerobically and in the a cellulose-rich environment has been undoubtedly fostered by the acquisition of foreign genes from bacterial neighbors, showing the global importance of such evolutionary mechanisms for successful eukaryotic thriving in such competitive environments.