The Mastigamoeba balamuthi genome and the nature of the free-living ancestor of Entamoeba

Žárský, Vojtěch, Klimeš, Vladimír, Pačes, Jan, Vlček, Čestmír, Hradilová, Miluše, Beneš, Vladimír, Nývltová, Eva, Hrdý, Ivan, Pyrih, Jan, Mach, Jan, Barlow, Lael, Stairs, Courtney W., Eme, Laura, Hall, Neil ORCID: https://orcid.org/0000-0003-2808-0009, Eliáš, Marek, Dacks, Joel B., Roger, Andrew and Tachezy, Jan (2021) The Mastigamoeba balamuthi genome and the nature of the free-living ancestor of Entamoeba. Molecular Biology and Evolution, 38 (6). 2240–2259. ISSN 0737-4038

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Abstract

The transition of free-living organisms to parasitic organisms is a mysterious process that occurs in all major eukaryotic lineages. Parasites display seemingly unique features associated with their pathogenicity; however, it is important to distinguish ancestral preconditions to parasitism from truly new parasite-specific functions. Here, we sequenced the genome and transcriptome of anaerobic free-living Mastigamoeba balamuthi and performed phylogenomic analysis of four related members of the Archamoebae, including Entamoeba histolytica, an important intestinal pathogen of humans. We aimed to trace gene histories throughout the adaptation of the aerobic ancestor of Archamoebae to anaerobiosis and throughout the transition from a free-living to a parasitic lifestyle. These events were associated with massive gene losses that, in parasitic lineages, resulted in a reduction in structural features, complete losses of some metabolic pathways, and a reduction in metabolic complexity. By reconstructing the features of the common ancestor of Archamoebae, we estimated preconditions for the evolution of parasitism in this lineage. The ancestor could apparently form chitinous cysts, possessed proteolytic enzyme machinery, compartmentalized the sulfate activation pathway in mitochondrion-related organelles, and possessed the components for anaerobic energy metabolism. After the split of Entamoebidae, this lineage gained genes encoding surface membrane proteins that are involved in host–parasite interactions. In contrast, gene gains identified in the M. balamuthi lineage were predominantly associated with polysaccharide catabolic processes. A phylogenetic analysis of acquired genes suggested an essential role of lateral gene transfer in parasite evolution (Entamoeba) and in adaptation to anaerobic aquatic sediments (Mastigamoeba).

Item Type: Article
Additional Information: The genomic sequences have been deposited in the online resource for community annotation of eukaryotes (ORCAE, https://bioinformatics.psb.ugent.be/orcae/overview/Masba).
Uncontrolled Keywords: archamoebae,mastigamoeba,chitinous cysts,evolution of parasitism,lateral gene transfer,pathway complexity,ecology, evolution, behavior and systematics,molecular biology,genetics ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 12 May 2021 00:21
Last Modified: 23 Oct 2022 02:19
URI: https://ueaeprints.uea.ac.uk/id/eprint/79981
DOI: 10.1093/molbev/msab020

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