Shining the spotlight on the neglected: new high-quality genome assemblies as a gateway to understanding the evolution of Trypanosomatidae.

Dixenous Genome assembly Monoxenous Parasite Protist Trypanosomatids Whole-genome sequencing

Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
21 Aug 2023
Historique:
received: 08 06 2023
accepted: 15 08 2023
medline: 23 8 2023
pubmed: 22 8 2023
entrez: 22 8 2023
Statut: epublish

Résumé

Protists of the family Trypanosomatidae (phylum Euglenozoa) have gained notoriety as parasites affecting humans, domestic animals, and agricultural plants. However, the true extent of the group's diversity spreads far beyond the medically and veterinary relevant species. We address several knowledge gaps in trypanosomatid research by undertaking sequencing, assembly, and analysis of genomes from previously overlooked representatives of this protistan group. We assembled genomes for twenty-one trypanosomatid species, with a primary focus on insect parasites and Trypanosoma spp. parasitizing non-human hosts. The assemblies exhibit sizes consistent with previously sequenced trypanosomatid genomes, ranging from approximately 18 Mb for Obscuromonas modryi to 35 Mb for Crithidia brevicula and Zelonia costaricensis. Despite being the smallest, the genome of O. modryi has the highest content of repetitive elements, contributing nearly half of its total size. Conversely, the highest proportion of unique DNA is found in the genomes of Wallacemonas spp., with repeats accounting for less than 8% of the assembly length. The majority of examined species exhibit varying degrees of aneuploidy, with trisomy being the most frequently observed condition after disomy. The genome of Obscuromonas modryi represents a very unusual, if not unique, example of evolution driven by two antidromous forces: i) increasing dependence on the host leading to genomic shrinkage and ii) expansion of repeats causing genome enlargement. The observed variation in somy within and between trypanosomatid genera suggests that these flagellates are largely predisposed to aneuploidy and, apparently, exploit it to gain a fitness advantage. High heterogeneity in the genome size, repeat content, and variation in chromosome copy numbers in the newly-sequenced species highlight the remarkable genome plasticity exhibited by trypanosomatid flagellates. These new genome assemblies are a robust foundation for future research on the genetic basis of life cycle changes and adaptation to different hosts in the family Trypanosomatidae.

Sections du résumé

BACKGROUND BACKGROUND
Protists of the family Trypanosomatidae (phylum Euglenozoa) have gained notoriety as parasites affecting humans, domestic animals, and agricultural plants. However, the true extent of the group's diversity spreads far beyond the medically and veterinary relevant species. We address several knowledge gaps in trypanosomatid research by undertaking sequencing, assembly, and analysis of genomes from previously overlooked representatives of this protistan group.
RESULTS RESULTS
We assembled genomes for twenty-one trypanosomatid species, with a primary focus on insect parasites and Trypanosoma spp. parasitizing non-human hosts. The assemblies exhibit sizes consistent with previously sequenced trypanosomatid genomes, ranging from approximately 18 Mb for Obscuromonas modryi to 35 Mb for Crithidia brevicula and Zelonia costaricensis. Despite being the smallest, the genome of O. modryi has the highest content of repetitive elements, contributing nearly half of its total size. Conversely, the highest proportion of unique DNA is found in the genomes of Wallacemonas spp., with repeats accounting for less than 8% of the assembly length. The majority of examined species exhibit varying degrees of aneuploidy, with trisomy being the most frequently observed condition after disomy.
CONCLUSIONS CONCLUSIONS
The genome of Obscuromonas modryi represents a very unusual, if not unique, example of evolution driven by two antidromous forces: i) increasing dependence on the host leading to genomic shrinkage and ii) expansion of repeats causing genome enlargement. The observed variation in somy within and between trypanosomatid genera suggests that these flagellates are largely predisposed to aneuploidy and, apparently, exploit it to gain a fitness advantage. High heterogeneity in the genome size, repeat content, and variation in chromosome copy numbers in the newly-sequenced species highlight the remarkable genome plasticity exhibited by trypanosomatid flagellates. These new genome assemblies are a robust foundation for future research on the genetic basis of life cycle changes and adaptation to different hosts in the family Trypanosomatidae.

Identifiants

pubmed: 37605127
doi: 10.1186/s12864-023-09591-z
pii: 10.1186/s12864-023-09591-z
pmc: PMC10441713
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

471

Subventions

Organisme : e-INFRA CZ
ID : 90140
Organisme : Russian Science Foundation
ID : 19-15-00054
Organisme : Russian Science Foundation
ID : 19-15-00054
Organisme : Grantová Agentura České Republiky
ID : 23-07695S
Organisme : Grantová Agentura České Republiky
ID : 22-14356S
Organisme : Grantová Agentura České Republiky
ID : 22-14356S
Organisme : Grantová Agentura České Republiky
ID : 23-07695S
Organisme : European Regional Funds
ID : CZ.02.1.01/16_019/ 0000759
Organisme : European Regional Funds
ID : CZ.02.1.01/16_019/ 0000759
Organisme : European Regional Funds
ID : CZ.02.1.01/16_019/ 0000759
Organisme : European Regional Funds
ID : CZ.02.1.01/16_019/ 0000759

Informations de copyright

© 2023. BioMed Central Ltd., part of Springer Nature.

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Auteurs

Amanda T S Albanaz (ATS)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00, Ostrava, Czech Republic.

Mark Carrington (M)

Department of Biochemistry, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QW, UK.

Alexander O Frolov (AO)

Zoological Institute of the Russian Academy of Sciences, 199034, St. Petersburg, Russia.

Anna I Ganyukova (AI)

Zoological Institute of the Russian Academy of Sciences, 199034, St. Petersburg, Russia.

Evgeny S Gerasimov (ES)

Faculty of Biology, M. V. Lomonosov Moscow State University, 119991, Moscow, Russia.
Martsinovsky Institute of Medical Parasitology, Sechenov University, 119435, Moscow, Russia.

Alexei Y Kostygov (AY)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00, Ostrava, Czech Republic.

Julius Lukeš (J)

Institute of Parasitology, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic.
Faculty of Sciences, University of South Bohemia, 370 05, České Budějovice, Czech Republic.

Marina N Malysheva (MN)

Zoological Institute of the Russian Academy of Sciences, 199034, St. Petersburg, Russia.

Jan Votýpka (J)

Institute of Parasitology, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic.
Department of Parasitology, Faculty of Science, Charles University, 128 44, Prague, Czech Republic.

Alexandra Zakharova (A)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00, Ostrava, Czech Republic.

Kristína Záhonová (K)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00, Ostrava, Czech Republic.
Institute of Parasitology, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic.
Department of Parasitology, Faculty of Science, Charles University, BIOCEV, 252 50, Vestec, Czech Republic.
Division of Infectious Diseases, Department of Medicine, University of Alberta, Edmonton, T6G 2G3, Canada.

Sara L Zimmer (SL)

Duluth Campus, University of Minnesota Medical School, Duluth, MN, 55812, USA.

Vyacheslav Yurchenko (V)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00, Ostrava, Czech Republic. vyacheslav.yurchenko@osu.cz.

Anzhelika Butenko (A)

Life Science Research Centre, Faculty of Science, University of Ostrava, 710 00, Ostrava, Czech Republic. anzhelika.butenko@paru.cas.cz.
Institute of Parasitology, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic. anzhelika.butenko@paru.cas.cz.
Faculty of Sciences, University of South Bohemia, 370 05, České Budějovice, Czech Republic. anzhelika.butenko@paru.cas.cz.

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