Annelid-Myxosporean Interactions

Alexander, Julie D.; Kerans, Billie L.; El‐Matbouli, Mansour; Hallett, Sascha L.; Stevens, Lori

doi:10.1007/978-3-319-14753-6_12

Cited by 16 publications

(16 citation statements)

References 123 publications

(89 reference statements)

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“…In its fish host, it undergoes proliferation and sporogenesis in pseudocysts within the white muscle (11), a tissue known to have anaerobic metabolism (24). While the obligate invertebrate host of H. salminicola is unknown, it is probably an annelid from the family Naididae, based on known life cycles of related myxozoans (25). Members of the Naididae can grow and reproduce in anoxic environments (26).…”

Section: Discussionmentioning

confidence: 99%

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

Yahalomi

Atkinson

Neuhof

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Although aerobic respiration is a hallmark of eukaryotes, a few unicellular lineages, growing in hypoxic environments, have secondarily lost this ability. In the absence of oxygen, the mitochondria of these organisms have lost all or parts of their genomes and evolved into mitochondria-related organelles (MROs). There has been debate regarding the presence of MROs in animals. Using deep sequencing approaches, we discovered that a member of the Cnidaria, the myxozoan Henneguya salminicola, has no mitochondrial genome, and thus has lost the ability to perform aerobic cellular respiration. This indicates that these core eukaryotic features are not ubiquitous among animals. Our analyses suggest that H. salminicola lost not only its mitochondrial genome but also nearly all nuclear genes involved in transcription and replication of the mitochondrial genome. In contrast, we identified many genes that encode proteins involved in other mitochondrial pathways and determined that genes involved in aerobic respiration or mitochondrial DNA replication were either absent or present only as pseudogenes. As a control, we used the same sequencing and annotation methods to show that a closely related myxozoan, Myxobolus squamalis, has a mitochondrial genome. The molecular results are supported by fluorescence micrographs, which show the presence of mitochondrial DNA in M. squamalis, but not in H. salminicola. Our discovery confirms that adaptation to an anaerobic environment is not unique to single-celled eukaryotes, but has also evolved in a multicellular, parasitic animal. Hence, H. salminicola provides an opportunity for understanding the evolutionary transition from an aerobic to an exclusive anaerobic metabolism.

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Section: Discussionmentioning

confidence: 99%

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

Yahalomi

Atkinson

Neuhof

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…The adoption of covert infection strategies by malacosporeans begs the question of whether periods of covert infection are also employed by other parasites of invertebrate hosts. Here we discuss this question specifically regarding their myxozoan relatives - the myxosporeans, whose life-cycles involve annelids as primary hosts [ 50 ]. This focus enables us to pursue comparative insights and thus to highlight key questions about covert infection strategies, impacts and effects.…”

Section: Discussionmentioning

confidence: 99%

“…PCR-based assays demonstrate that M. cerebralis prevalences in T. tubifex populations are usually < 10% and typically < 1% (e.g. [ 50 , 52 , 53 ]). Whether such covert infections are generally avirulent like those characterised for malacosporeans in bryozoan hosts remains unknown.…”

Section: Discussionmentioning

confidence: 99%

Persistence, impacts and environmental drivers of covert infections in invertebrate hosts

et al. 2017

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BackgroundPersistent covert infections of the myxozoan, Tetracapsuloides bryosalmonae, in primary invertebrate hosts (the freshwater bryozoan, Fredericella sultana) have been proposed to represent a reservoir for proliferative kidney disease in secondary fish hosts. However, we have limited understanding of how covert infections persist and vary in bryozoan populations over time and space and how they may impact these populations. In addition, previous studies have likely underestimated covert infection prevalence. To improve our understanding of the dynamics, impacts and implications of covert infections we employed a highly sensitive polymerase chain reaction (PCR) assay and undertook the first investigation of covert infections in the field over an annual period by sampling bryozoans every 45 days from three populations within each of three rivers.ResultsCovert infections persisted throughout the year and prevalence varied within and between rivers, but were often > 50%. Variation in temperature and water chemistry were linked with changes in prevalence in a manner consistent with the maintenance of covert infections during periods of low productivity and thus poor growth conditions for both bryozoans and T. bryosalmonae. The presence and increased severity of covert infections reduced host growth but only when bryozoans were also investing in the production of overwintering propagules (statoblasts). However, because statoblast production is transitory, this effect is unlikely to greatly impact the capacity of bryozoan populations to act as persistent sources of infections and hence potential disease outbreaks in farmed and wild fish populations.ConclusionsWe demonstrate that covert infections are widespread and persist over space and time in bryozoan populations. To our knowledge, this is the first long-term study of covert infections in a field setting. Review of the results of this and previous studies enables us to identify key questions related to the ecology and evolution of covert infection strategies and associated host-parasite interactions.Electronic supplementary materialThe online version of this article (10.1186/s13071-017-2495-8) contains supplementary material, which is available to authorized users.

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“…Myxosporean plasmodia and pseudoplasmodia are generally tiny, but some are mm to cm in dimensions. Annelid hosts of myxosporeans are mostly unknown -infections so far have been detected in 7 (Alexander et al 2015) of approximately 120 families (Fauchald and Rouse 1997;Erséus 2005). Fish are widely exploited by myxosporeans with infections reported in many familes of both cartilaginous and bony fishes.…”

Section: Fishmentioning

confidence: 99%

“…El-Matbouli and Hoffmann 1998; Bartholomew et al 1997). Pathological effects on annelid hosts include tissue damage, reduced fecundity and hypertrophic growth (Elwell et al 2009;Alexander et al 2015) -as occurs in infected phylactolaemate bryozoans (see below). In general, myxozoan stages are unlikely to be preserved in fossil annelids, however, soft-body features are clearly recognisable in several exceptional preservations (e.g.…”

Section: Annelid Origins and Fossil Recordmentioning

confidence: 99%

Evolution, Origins and Diversification of Parasitic Cnidarians

Okamura¹,

Gruhl²

2020

Preprint

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Parasitism has evolved in cnidarians on multiple occasions but only one clade – the Myxozoa – has undergone substantial radiation. We briefly review minor parasitic clades that exploit pelagic hosts and then focus on the comparative biology and evolution of the highly speciose Myxozoa and its monotypic sister taxon, Polypodium hydriforme, which collectively form the Endocnidozoa. Cnidarian features that may have facilitated the evolution of endoparasitism are highlighted before considering endocnidozoan origins, life cycle evolution and potential early hosts. We review the fossil evidence and evaluate existing inferences based on molecular clock and co-phylogenetic analyses. Finally, we consider patterns of adaptation and diversification and stress how poor sampling might preclude adequate understanding of endocnidozoan diversity.

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Annelid-Myxosporean Interactions

Cited by 16 publications

References 123 publications

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome

Persistence, impacts and environmental drivers of covert infections in invertebrate hosts

Evolution, Origins and Diversification of Parasitic Cnidarians

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