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Identification of a new gregarine parasite associated with mass mortality events of freshwater pearl mussels (Margaritifera margaritifera) in Sweden
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Systematic Biology. Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute (SVA), Uppsala, Sweden.ORCID iD: 0000-0003-1733-4085
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Natural History Museum, University of Oslo, Oslo, Norway.ORCID iD: 0000-0002-7723-8629
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2024 (English)In: Journal of Eukaryotic Microbiology, ISSN 1066-5234, E-ISSN 1550-7408, Vol. 71, no 3, article id e13021Article in journal (Refereed) Published
Abstract [en]

Freshwater bivalves play key ecological roles in lakes and rivers, largely contributing to healthy ecosystems. The freshwater pearl mussel, Margaritifera margaritifera, is found in Europe and on the East coast of North America. Once common in oxygenated streams, M. margaritifera is rapidly declining and consequently assessed as a threatened species worldwide. Deterioration of water quality has been considered the main factor for the mass mortality events affecting this species. Yet, the role of parasitic infections has not been investigated. Here, we report the discovery of three novel protist lineages found in Swedish populations of M. margaritifera belonging to one of the terrestrial groups of gregarines (Eugregarinorida, Apicomplexa). These lineages are closely related–but clearly separated–from the tadpole parasite Nematopsis temporariae. In one lineage, which is specifically associated with mortality events of M. margaritifera, we found cysts containing single vermiform zoites in the gills and other organs of diseased individuals using microscopy and in situ hybridization. This represents the first report of a parasitic infection in M. margaritifera that may be linked to the decline of this mussel species. We propose a tentative life cycle with the distribution of different developmental stages and potential exit from the host into the environment.

Place, publisher, year, edition, pages
John Wiley & Sons, 2024. Vol. 71, no 3, article id e13021
Keywords [en]
freshwater perl mussel, gregarine, ISH, Margaritifera margaritifera, mass mortality, mortality, Nematopsis, pathology, phylogeny, TEM
National Category
Ecology
Identifiers
URN: urn:nbn:se:uu:diva-446934DOI: 10.1111/jeu.13021ISI: 001184534000001OAI: oai:DiVA.org:uu-446934DiVA, id: diva2:1571503
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
Science for Life Laboratory, SciLifeLabSwedish Research Council Formas, 2017-01197Swedish Research Council, 2018-0597Swedish Research Council, 2017-04563
Note

Authors and title in the list of papers of Mahwash Jamy's thesis: Alfjorden, A., Brännström, I. O., Wengström, N., Jamy, M., Kristmundson, A., Jansson, E., Burki, F. Identification of a new gregarine parasite [Apicomplexa, Alveolata] in mass mortality events of freshwater pearl mussels (Margaritifera margaritifera)

Available from: 2021-06-22 Created: 2021-06-22 Last updated: 2024-09-20Bibliographically approved
In thesis
1. Environmental sequencing to infer patterns of eukaryotic evolution: Combining long-read and short-read metabarcoding
Open this publication in new window or tab >>Environmental sequencing to infer patterns of eukaryotic evolution: Combining long-read and short-read metabarcoding
2021 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Our view of eukaryotes is biased towards plants, animals, and fungi. But the vast majority of eukaryotic diversity is microbial in nature. These microbial eukaryotes are key players in all ecosystems on earth and are collectively known as protists. Over the past decade we have gathered a better understanding of environmental protist diversity and ecology through metabarcoding studies, which routinely generate millions of reads corresponding to short fragments (< 500 bp) of the 18S gene. However, the limited phylogenetic signal of these short reads hinders their use in investigating questions of an evolutionary nature. 

To overcome this limitation, we introduced a method for long-read metabarcoding in Paper I of this thesis. We validated this method by amplifying DNA from three soil samples and sequencing with PacBio to obtain a ca. 4500 bp region of the ribosomal DNA operon spanning the 18S and 28S genes. The long-reads were taxonomically annotated using a phylogeny-aware approach, and were used to infer robust 18S-28S phylogenies of the environmental diversity. 

In Paper II, we investigated habitat evolution across the eukaryotic tree of life, using a unique combination of long-read and short-read metabarcoding data in a phylogenetic framework. We showed that transitions across the marine-terrestrial habitat boundary are more frequent than previously assumed, and that eukaryotic groups vary in their ability to cross this habitat boundary. We inferred that the last eukaryotic common ancestor inhabited non-marine environments, and that subsequent transitions across the marine-terrestrial boundary likely played a key role in eukaryotic evolution by opening new niches to fill.

Paper III focused on determining the effects of habitat and latitude on the rates of molecular evolution of protists. Analyses on phylogenies inferred from long-read metabarcoding data found no systematic differences in the evolutionary rates of marine and terrestrial species. Additionally, contrary to expectations, not all eukaryotic groups showed an increase in evolutionary rates towards the equator, with some groups displaying the opposite trend. 

Finally Paper IV isolates the parasite of the endangered freshwater pearl mussel in Sweden, and phylogenetic analyses including long-read metabarcoding data identifies it as a gregarine belonging to the genus Nematopsis. 

In summary, this thesis introduces a new method for environmental sequencing of protists, and urges future studies to use both long-read and short-read metabarcoding data to study outstanding questions in eukaryotic evolution and ecology. 

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2021. p. 70
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2054
Keywords
Protists, eukaryotes, environmental sequencing, ribosomal DNA, PacBio, long-read metabarcoding, phylogenetics, salt barrier, habitat evolution, eukaryotes evolution, evolutionary rate, Apicomplexa, pathogen
National Category
Biological Sciences
Research subject
Biology with specialization in Systematics
Identifiers
urn:nbn:se:uu:diva-446935 (URN)978-91-513-1242-2 (ISBN)
Public defence
2021-09-10, Ekmansalen, Evolutionary Biology Centre (EBC), Norbyvägen 14, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2021-08-13 Created: 2021-06-22 Last updated: 2021-08-25
2. 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)
Opponent
Supervisors
Available from: 2024-10-11 Created: 2024-09-18 Last updated: 2024-10-31

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Alfjorden, AndersOnut-Brännström, IoanaJamy, MahwashBurki, Fabien

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