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


Journal

Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455

Informations de publication

Date de publication:
19 05 2021
Historique:
pubmed: 3 2 2021
medline: 12 8 2021
entrez: 2 2 2021
Statut: ppublish

Résumé

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).

Identifiants

pubmed: 33528570
pii: 6126414
doi: 10.1093/molbev/msab020
pmc: PMC8136499
doi:

Types de publication

Comparative Study Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2240-2259

Informations de copyright

© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Auteurs

Vojtěch Žárský (V)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.

Vladimír Klimeš (V)

Department of Biology and Ecology, Faculty of Science, University of Ostrava, Ostrava, Czech Republic.

Jan Pačes (J)

Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Prague, Czech Republic.

Čestmír Vlček (Č)

Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Prague, Czech Republic.

Miluše Hradilová (M)

Institute of Molecular Genetics, Academy of Sciences of the Czech Republic, Prague, Czech Republic.

Vladimír Beneš (V)

European Molecular Biology Laboratory (EMBL), Genomics Core Facility, Heidelberg, Germany.

Eva Nývltová (E)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.

Ivan Hrdý (I)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.

Jan Pyrih (J)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.

Jan Mach (J)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.

Lael Barlow (L)

Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada.

Courtney W Stairs (CW)

Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada.
Department of Cell and Molecular Biology, Uppsala University, Uppsala, Sweden.

Laura Eme (L)

Diversity, Ecology and Evolution of Microbes (DEEM), Unité Ecologie Systématique Evolution Université Paris-Saclay, Orsay, France.

Neil Hall (N)

The Earlham Institute, Norwich Research Park, Norwich, United Kingdom.
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, United Kingdom.

Marek Eliáš (M)

Department of Biology and Ecology, Faculty of Science, University of Ostrava, Ostrava, Czech Republic.

Joel B Dacks (JB)

Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada.
Division of Infectious Diseases, Department of Medicine, University of Alberta, Edmonton, AB, Canada.
Institute of Parasitology, Biology Centre, CAS, v.v.i., Ceske Budejovice, Czech Republic.

Andrew Roger (A)

Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada.

Jan Tachezy (J)

Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Vestec, Czech Republic.

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