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Comparative genomics of Ascetosporea gives new insight into the evolutionary basis for animal parasitism in Rhizaria
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.ORCID iD: 0000-0002-8880-872X
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology.ORCID iD: 0000-0003-1733-4085
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2024 (English)In: BMC Biology, E-ISSN 1741-7007, Vol. 22, no 1, article id 103Article in journal (Refereed) Published
Abstract [en]

Background

Ascetosporea (Endomyxa, Rhizaria) is a group of unicellular parasites infecting aquatic invertebrates. They are increasingly being recognized as widespread and important in marine environments, causing large annual losses in invertebrate aquaculture. Despite their importance, little molecular data of Ascetosporea exist, with only two genome assemblies published to date. Accordingly, the evolutionary origin of these parasites is unclear, including their phylogenetic position and the genomic adaptations that accompanied the transition from a free-living lifestyle to parasitism. Here, we sequenced and assembled three new ascetosporean genomes, as well as the genome of a closely related amphizoic species, to investigate the phylogeny, origin, and genomic adaptations to parasitism in Ascetosporea.

Results

Using a phylogenomic approach, we confirm the monophyly of Ascetosporea and show that Paramyxida group with Mikrocytida, with Haplosporida being sister to both groups. We report that the genomes of these parasites are relatively small (12–36 Mb) and gene-sparse (~ 2300–5200 genes), while containing surprisingly high amounts of non-coding sequence (~ 70–90% of the genomes). Performing gene-tree aware ancestral reconstruction of gene families, we demonstrate extensive gene losses at the origin of parasitism in Ascetosporea, primarily of metabolic functions, and little gene gain except on terminal branches. Finally, we highlight some functional gene classes that have undergone expansions during evolution of the group.

Conclusions

We present important new genomic information from a lineage of enigmatic but important parasites of invertebrates and illuminate some of the genomic innovations accompanying the evolutionary transition to parasitism in this lineage. Our results and data provide a genetic basis for the development of control measures against these parasites.

Place, publisher, year, edition, pages
BioMed Central (BMC), 2024. Vol. 22, no 1, article id 103
Keywords [en]
Genome reduction, Reductive evolution, Evolutionary transition, Phylogeny, Protozoa, Intracellular parasite, Bonamia, Marteilia, Paramarteilia, Mikrocytos, Paramikrocytos
National Category
Evolutionary Biology Genetics
Identifiers
URN: urn:nbn:se:uu:diva-538616DOI: 10.1186/s12915-024-01898-xISI: 001214191700002PubMedID: 38702750OAI: oai:DiVA.org:uu-538616DiVA, id: diva2:1898804
Part of project
Parasites in the environment: detection and diagnostics of emerging disease agents in aquaculture, Swedish Research Council FormasEvolution of ascetosporean parasites, an emerging threat in marine environments, Swedish Research Council
Funder
Swedish Research Council, 2017-04563Science for Life Laboratory, SciLifeLabSwedish Research Council Formas, 2017-01197Stockholm UniversityAvailable from: 2024-09-18 Created: 2024-09-18 Last updated: 2024-09-18Bibliographically approved
In thesis
1. Morphological and molecular studies of bivalves to assess the hidden diversity of protistan parasites: Investigations of cryptic diseases in shellfish
Open this publication in new window or tab >>Morphological and molecular studies of bivalves to assess the hidden diversity of protistan parasites: Investigations of cryptic diseases in shellfish
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis investigates the host - parasitic relationships in mussel, started by investigating unexplained massmortalities in freshwater mussels, Margaritifera margaritifera. By compiling geodata with symptoms and histopathology (Paper 1). In Paper 2, I continued on these investigations, describing a parasitic gregarines in host. Using in situ hybridization (ISH) and ultrastructural analysis, we linked this gregarine to host detected lesions. To investigate fixed sampled, we used CARD-FISH demonstrating new patterns of parasitic infiltration of gonads. (Paper 3). In marine environments, protist parasites have been throughly documented, though several lesions remain unexplained. Using cell culture, we isolated Hexamita nelsoni linking this protist with blue mussels lesions in muscle & gonads, using CARD-FISH (Paper 4). The largest threat towards marine mussel aquaculture are Ascetosporean parasites, not culturable, requiring alternative methods for genomic studies. We used, density gradient filtration to concentrate Marteilia pararefringens and Bonamia ostreae from infected tissues, enabling these studies, Paper 5.

Abstract [sv]

Mitt doktorandsarbete undersöker relationen mellan musslan och dessa parasiter. Arbetet startade med studier av oförklarade massdödligheter bland sötvattens musslor, Margaritifera margaritifera, genom sammanställning av geologiska data och observerade sjukdomssymtom (Paper 1). In nästa studie (Paper 2), fortsätter vi detta genom att beskriva en ny gregarin (Apicomplexa) associerade med organförändringar. Med In situ hybridisering (ISH) och elektronmikroskopi, kunde vi koppla dessa till observerade vävnadsskador. Vidare påvisade vi olika arter av gregariner genom CARD-FISH metodik i histologiska prover och demonstrera därigenom nya mönster av parasitär infiltration (Paper 3). Mussel parasiter i marin miljö är  väldokumenterade, även om vissa organskador förblivit oförklarade. Genom cellkultur från blåmussla isolerades Hexamita nelsoni, och kopplades till observerade organskador, i muskel och gonadvävnad, med CARD-FISH (Paper 4). Det största hoten mot vattenbruk av Bivalver är Ascetosporea parasiter, som ej går at odla. För genomisk undersökning krävs andra alternativ. Med gradient filtrering  möjliggjordes koncentration av dessa celler och genomiska studier av Marteilia och Bonamia.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2024. p. 69
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2450
Keywords
Margaritifera margaritifera, Freshwater Pearl Mussel, Mass mortality events, Gregarine, Pathology, CARD-FISH, ISH, Mytilus edulis, blåmussla, Hexamita nelsoni, phylogeny, histology
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-538623 (URN)978-91-513-2233-9 (ISBN)
Public defence
2024-11-01, Lindahlsalen, 05.01058, Evolutionsbiologiskt centrum (EBC), Norbyvägen 14, Uppsala, 09:15 (English)
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Supervisors
Available from: 2024-10-11 Created: 2024-09-18 Last updated: 2024-10-31

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Hiltunen Thorén, MarkusOnuț-Brännström, IoanaAlfjorden, AndersBurki, Fabien

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