Mitochondrial genome sequencing of marine leukemias reveals cancer contagion between clam species in the Seas of Southern Europe

García‐Souto, Daniel; Al, Bruzos; Díaz, Seila; Rocha, Sara; Pequeno, Alberto; Cf, Roman-Lewis; Alonso, Juana; Rodríguez, Rosana López; Costas, Damián; Rodríguez-Castro, Jorge Homero; Villanueva, Antonio; L, Silva; Jm, Valencia; Annona, Giovanni; Tarallo, Andrea; Ricardo, Fernando; Ab, Cetinic; Posada, David; Pasantes, Juan J.; Jmc, Tubio

doi:10.1101/2021.03.10.434714

Cited by 6 publications

(8 citation statements)

References 28 publications

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“…Transmissible cancers are malignant cell lines, derived from a founder host, which can spread and colonize other individuals by transmission of living cancer cells. Several lineages of transmissible cancer have been described: one in dogs (canine transmissible venereal tumour, CTVT, Murgia et al, 2006; Rebbeck et al, 2009), two in Tasmanian devils (devil facial tumour disease, DFT1 and 2, Pearse & Swift, 2006; Pye et al, 2016) and, more recently, seven in different bivalve species (bivalve transmissible neoplasia, BTN, Garcia‐Souto et al, 2021; Metzger et al, 2015, 2016; Yonemitsu et al, 2019). The three lineages found in vertebrates are the best studied to date.…”

Section: Introductionmentioning

confidence: 99%

Prevalence and polymorphism of a mussel transmissible cancer in Europe

et al. 2021

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Transmissible cancers are parasitic malignant cell lineages that acquired the ability to infect new hosts from the same species, or sometimes related species. First described in dogs and Tasmanian devils, transmissible cancers were later discovered in some marine bivalves affected by a leukemia-like disease. In Mytilus mussels, two lineages of Bivalve Transmissible Neoplasia (BTN) have been described to date (MtrBTN1 and MtrBTN2), both emerged in a M. trossulus founder individual. Here, we performed an extensive screening of genetic chimerism, a hallmark of transmissible cancer, by genotyping 106 SNPs of 5907 European Mytilus mussels. The genetic analysis allowed us to simultaneously obtain the genotype of hosts -M. edulis, M. galloprovincialis or hybrids -and the genotype of tumors of heavily infected individuals. In addition, a subset of 222 individuals were systematically genotyped and analysed by histology in order to screen for possible non-transmissible cancers. We detected MtrBTN2 at low prevalence in M.edulis, and also in M. galloprovincialis and hybrids although at a much lower prevalence. No MtrBTN1 or new BTN were found, but 8 individuals with non-transmissible neoplasia were observed at a single polluted site on the same sampling date. We observed a diversity of MtrBTN2 genotypes that appeared more introgressed or more ancestral than MtrBTN1 and reference healthy M. trossulus individuals. The observed polymorphism is most likely due to somatic null alleles caused by structural variations or point mutations in primer-binding sites leading to enhanced detection of the host alleles. Despite low prevalence, two sublineages divergent by 10% fixed somatic null alleles and one non-synonymous mtCOI substitution, are co-spreading in the same geographic area, suggesting a complex diversification of MtrBTN2 since its emergence and host species shift.

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Section: Introductionmentioning

confidence: 99%

Prevalence and polymorphism of a mussel transmissible cancer in Europe

et al. 2021

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“…The transmissibility of these cancerous cell lines has been demonstrated through i) the presence of genetic chimerism in the diseased animals, with genetic differences between tumor and host cells, and (ii) the genetic similarity between tumors of different individuals. To date, several lineages of transmissible cancers have been described: one in dogs (Canine Transmissible Venereal Tumor, CTVT 7 , 8 , two in Tasmanian devils (Devil Facial Tumor Disease, DFT1 and 2 9 , 10 , and seven in various bivalve families (Bivalve Transmissible Neoplasia, BTN) 11 – 14 . Among BTNs, MtrBTN1 and MtrBTN2 are two distinct lineages with a Mytilus trossulus origin that infect mussel species of the genus Mytilus .…”

Section: Introductionmentioning

confidence: 99%

Traits of a mussel transmissible cancer are reminiscent of a parasitic life style

Burioli

Hammel

Bierne

et al. 2021

Sci Rep

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Some cancers have evolved the ability to spread from host to host by transmission of cancerous cells. These rare biological entities can be considered parasites with a host-related genome. Still, we know little about their specific adaptation to a parasitic lifestyle. MtrBTN2 is one of the few lineages of transmissible cancers known in the animal kingdom. Reported worldwide, MtrBTN2 infects marine mussels. We isolated MtrBTN2 cells circulating in the hemolymph of cancerous mussels and investigated their phenotypic traits. We found that MtrBTN2 cells had remarkable survival capacities in seawater, much higher than normal hemocytes. With almost 100% cell survival over three days, they increase significantly their chances to infect neighboring hosts. MtrBTN2 also triggered an aggressive cancerous process: proliferation in mussels was ~ 17 times higher than normal hemocytes (mean doubling time of ~ 3 days), thereby favoring a rapid increase of intra-host population size. MtrBTN2 appears to induce host castration, thereby favoring resources re-allocation to the parasites and increasing the host carrying capacity. Altogether, our results highlight a series of traits of MtrBTN2 consistent with a marine parasitic lifestyle that may have contributed to the success of its persistence and dissemination in different mussel populations across the globe.

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“…To date, seven lineages of the bivalve transmissible neoplasia (BTN) in eight bivalve species have been reported (5,(12)(13)(14)(15)(16)(17). In many cases, the BTN that circulates in each species has arisen from a member of that same species.…”

Section: Introductionmentioning

confidence: 99%

“…DN was first confirmed to be a transmissible cancer in soft-shell clams ( Mya arenaria ) (5), and later, multiple independent lineages of transmissible cancer were identified in multiple species worldwide (12). To date, seven lineages of the bivalve transmissible neoplasia (BTN) in eight bivalve species have been reported (5, 12–17). In many cases, the BTN that circulates in each species has arisen from a member of that same species.…”

Section: Introductionmentioning

confidence: 99%

Survival and detection of bivalve transmissible neoplasia from the soft-shell clam Mya arenaria (MarBTN) in seawater

Giersch

Hart

Reddy³

et al. 2021

Preprint

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Many pathogens can cause cancer, but cancer itself does not normally act as an infectious agent. However, transmissible cancers have been found in a few cases in nature: in Tasmanian devils, dogs, and several bivalve species. The transmissible cancers in dogs and devils are known to spread through direct physical contact, but the exact route of transmission of bivalve transmissible neoplasia (BTN) has not yet been confirmed. It has been hypothesized that cancer cells could be released by diseased animals and spread through the water column to infect/engraft into other animals. To test the feasibility of this proposed mechanism of transmission, we tested the ability of BTN cells from the soft-shell clam (Mya arenaria BTN, or MarBTN) to survive in artificial seawater. We found that BTN cells are highly sensitive to salinity, with acute toxicity at salinity levels lower than those found in their environment. BTN cells also survive longer at lower temperatures, with >48% of cells surviving a week in seawater at temperatures from 4°C to 16°C, and 49% surviving for more than two weeks at 4°C. With one clam donor, living cells were observed for more than eight weeks at 4°C. We also used qPCR of environmental DNA (eDNA) to detect the presence of BTN-specific DNA in the environment. We observed release of BTN-specific DNA into the water of aquaria from tanks with highly BTN-positive clams, and we detected BTN-specific DNA in seawater samples collected from BTN-endemic areas, although the level detected was much lower. Overall, these data show that BTN cells can survive well in seawater, and they are released into the water by diseased animals, supporting the hypothesis that BTN is spread from animal-to-animal by cells through seawater.

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Mitochondrial genome sequencing of marine leukemias reveals cancer contagion between clam species in the Seas of Southern Europe

Cited by 6 publications

References 28 publications

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Prevalence and polymorphism of a mussel transmissible cancer in Europe

Traits of a mussel transmissible cancer are reminiscent of a parasitic life style

Survival and detection of bivalve transmissible neoplasia from the soft-shell clam Mya arenaria (MarBTN) in seawater

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