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The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba

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 tru...

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Autores principales: 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, Eliáš, Marek, Dacks, Joel B, Roger, Andrew, Tachezy, Jan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136499/
https://www.ncbi.nlm.nih.gov/pubmed/33528570
http://dx.doi.org/10.1093/molbev/msab020
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author 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
Eliáš, Marek
Dacks, Joel B
Roger, Andrew
Tachezy, Jan
author_facet 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
Eliáš, Marek
Dacks, Joel B
Roger, Andrew
Tachezy, Jan
author_sort Žárský, Vojtěch
collection PubMed
description 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).
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spelling pubmed-81364992021-05-25 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 Eliáš, Marek Dacks, Joel B Roger, Andrew Tachezy, Jan Mol Biol Evol Discoveries 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). Oxford University Press 2021-02-02 /pmc/articles/PMC8136499/ /pubmed/33528570 http://dx.doi.org/10.1093/molbev/msab020 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
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
Eliáš, Marek
Dacks, Joel B
Roger, Andrew
Tachezy, Jan
The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
title The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
title_full The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
title_fullStr The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
title_full_unstemmed The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
title_short The Mastigamoeba balamuthi Genome and the Nature of the Free-Living Ancestor of Entamoeba
title_sort mastigamoeba balamuthi genome and the nature of the free-living ancestor of entamoeba
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136499/
https://www.ncbi.nlm.nih.gov/pubmed/33528570
http://dx.doi.org/10.1093/molbev/msab020
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