Abstract:Disseminated neoplasia (DN) is one of the most challenging and unrecognised diseases occurring in aquatic fauna. It has been diagnosed in four bivalve species from the Gulf of Gdańsk (Southern Baltic Sea) with the highest frequency in Macoma balthica (formerly Limecola balthica), reaching up to 94% in some populations. The aetiology of DN in the Baltic Sea has not yet been identified, with earlier studies trying to link its occurrence with environmental pollution. Taking into account recent research providing … Show more
“…Transmissible cancers are malignant cell lineages that have acquired the ability to infect new hosts through the transmission of living cancer cells. Eleven transmissible cancer lineages have been described to date: one in dogs (canine transmissible venereal tumour, CTVT [1,2]), two in Tasmanian devils (devil facial tumour, DFT1 and DFT2 [3,4]), and eight in different marine bivalve species (bivalve transmissible neoplasia, BTNs [5][6][7][8][9]).…”
Transmissible cancer, a unique form of microparasites that spreads through direct transmission of living cancer cells, is increasingly reported in marine bivalves. In this study, we sought to understand the ecology of the propagation of Mytilus trossulus Bivalve Transmissible Neoplasia 2 (MtrBTN2), a transmissible cancer affecting four Mytilus mussel species worldwide. We investigated the prevalence of MtrBTN2 in the mosaic hybrid zone of M. edulis and M. galloprovincialis along the French Atlantic coast, sampling contrasting natural and anthropogenic habitats. We observed a similar prevalence in both species, likely due to the proximity of the two species in this region. Our results showed that ports had higher prevalence of MtrBTN2, with a hotspot observed at a shuttle landing dock. No cancer was found in natural beds except for two sites around the hotspot, suggesting spillover. Ports may provide favourable conditions for the transmission of MtrBTN2, such as high mussel density, confined sheltered shores, or buffered temperatures. Ships may also spread the disease through biofouling, with maritime traffic being the best predictor of MtrBTN2 prevalence. Our results suggest ports may serve as epidemiological hubs, with maritime routes providing artificial gateways for MtrBTN2 propagation. This highlights the importance of preventing biofouling on docks and ships hulls to limit the spread of marine pathogens.
“…Transmissible cancers are malignant cell lineages that have acquired the ability to infect new hosts through the transmission of living cancer cells. Eleven transmissible cancer lineages have been described to date: one in dogs (canine transmissible venereal tumour, CTVT [1,2]), two in Tasmanian devils (devil facial tumour, DFT1 and DFT2 [3,4]), and eight in different marine bivalve species (bivalve transmissible neoplasia, BTNs [5][6][7][8][9]).…”
Transmissible cancer, a unique form of microparasites that spreads through direct transmission of living cancer cells, is increasingly reported in marine bivalves. In this study, we sought to understand the ecology of the propagation of Mytilus trossulus Bivalve Transmissible Neoplasia 2 (MtrBTN2), a transmissible cancer affecting four Mytilus mussel species worldwide. We investigated the prevalence of MtrBTN2 in the mosaic hybrid zone of M. edulis and M. galloprovincialis along the French Atlantic coast, sampling contrasting natural and anthropogenic habitats. We observed a similar prevalence in both species, likely due to the proximity of the two species in this region. Our results showed that ports had higher prevalence of MtrBTN2, with a hotspot observed at a shuttle landing dock. No cancer was found in natural beds except for two sites around the hotspot, suggesting spillover. Ports may provide favourable conditions for the transmission of MtrBTN2, such as high mussel density, confined sheltered shores, or buffered temperatures. Ships may also spread the disease through biofouling, with maritime traffic being the best predictor of MtrBTN2 prevalence. Our results suggest ports may serve as epidemiological hubs, with maritime routes providing artificial gateways for MtrBTN2 propagation. This highlights the importance of preventing biofouling on docks and ships hulls to limit the spread of marine pathogens.
“…Despite several BTN clones having been newly described in recent years (9)(10)(11)(12)(13)(14), no analyses of whole BTN genomes have yet been reported. Combining a range of approaches, our study provides a first outlook into the genomes of these singular marine leukaemias in European common cockles, complementing the work of Hart et al (30) on American soft-shell clams.…”
Section: Discussionmentioning
confidence: 99%
“…Transmissible cancers are clonal somatic cell lineages that spread between individuals via direct transfer of living tumour cells, in a process analogous to cancer metastasis (1,2). Naturally occurring transmissible cancers have been identified in dogs (3)(4)(5), Tasmanian devils (6)(7)(8) and, more recently, several species of marine bivalve molluscs (9)(10)(11)(12)(13)(14). To date, eight transmissible cancer lineages, collectively known as bivalve transmissible neoplasia (BTN), have been described in bivalves, probably spreading via transfer of free-floating cells in seawater.…”
Transmissible cancers are malignant cell clones that spread among individuals through transfer of living cancer cells. Several such cancers, collectively known as bivalve transmissible neoplasia (BTN), are known to infect and cause leukaemia in marine bivalve molluscs. This is the case of BTN clones affecting the common cockle, Cerastoderma edule, which inhabits the Atlantic coasts of Europe and north-west Africa. To investigate the origin and evolution of contagious cancers in common cockles, we collected 6,854 C. edule specimens and diagnosed 390 cases of BTN. We then generated a reference genome for the species and assessed genomic variation in the genomes of 61 BTN tumours. Analysis of tumour-specific variants confirmed the existence of two cockle BTN lineages with independent clonal origins, and gene expression patterns supported their status as haemocyte-derived marine leukaemias. Examination of mitochondrial DNA sequences revealed several mitochondrial capture events in BTN, as well as co-infection of cockles by different tumour lineages. Mutational analyses identified two lineage-specific mutational signatures, one of which resembles a signature associated with DNA alkylation. Karyotypic and copy number analyses uncovered genomes marked by pervasive instability and polyploidy. Whole-genome duplication, amplification of oncogenes CCND3 and MDM2, and deletion of the DNA alkylation repair gene MGMT, are likely drivers of BTN evolution. Characterization of satellite DNA identified elements with vast expansions in the cockle germ line, yet absent from BTN tumours, suggesting ancient clonal origins. Our study illuminates the evolution of contagious cancers under the sea, and reveals long-term tolerance of extreme instability in neoplastic genomes.
“…Discovered in the past decade (Metzger et al, 2015, 2016), BTN lineages, the unicellular parasitic species of Bivalvia, are an unchartered component of marine diversity. Eight independent BTN lineages affecting nine different species are known (Garcia-Souto et al, 2021; Hammel et al, 2021; Metzger et al, 2015, 2016; Michnowska et al, 2022; Skazina et al, 2021; Yonemitsu et al, 2019). As an infectious disease, BTN is a threat to natural and commercial shellfish populations (Metzger et al, 2015, 2016 and references therein).…”
Bivalve transmissible neoplasia (BTN) is a leukemia-like cancer "metastasizing" by transmission of living cancer cells between molluscs. Blue mussels harbor two evolutionary lineages of BTN,MtrBTN1 andMtrBTN2, both derived fromMytilus trossulus. WhileMtrBTN1 has been found only inM. trossulusin North Pacific,MtrBTN2 parasitizes different Mytilus species worldwide, particularly in Western Europe. No targeted studies of BTN in Northern European mussels (M. edulis,M. trossulus) have been made. We searched for BTN in mussels from the Kola Bay (Barents Sea) with the help of flow cytometry of the hemolymph, qPCR with primers specific to cancer-associated alleles and sequencing of mitochondrial and nuclear loci. The species of the mussel hosts was ascertained genetically. BothMtrBTN1 andMtrBTN2 were present in our material, though their prevalence was low (~0.4%). The only instance ofMtrBTN2 was found inM. trossulus.MtrBTN1 occurred inM. trossulusand in a hybrid betweenM. trossulusandM. edulis. This finding indicates thatMtrBTN1 may potentially infect the latter species. The mtDNA haplotypes found in both lineages were nearly identical to those known from the North Pacific, but not from elsewhere. Our results suggest that they arrived in the Kola Bay fairly recently, probably with the maritime transport along the Northern Sea Route, and that the invasion was independent of that in Western Europe. A relatively young evolutionary age ofMtrBTN1 seems to suggest that it is an emerging disease in the process of niche expansion.
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