Genetic signature analysis of Perkinsus marinus in Mexico suggests possible translocation from the Atlantic Ocean to the Pacific coast of Mexico

Abstract

BackgroundThe protozoan Perkinsus marinus (Mackin, Owen & Collier) Levine, 1978 causes perkinsosis in the American oyster Crassostrea virginica Gmelin, 1791. This pathogen is present in cultured C. virginica from the Gulf of Mexico and has been reported recently in Saccostrea palmula (Carpenter, 1857), Crassostrea corteziensis (Hertlein, 1951) and Crassostrea gigas (Thunberg, 1793) from the Mexican Pacific coast. Transportation of fresh oysters for human consumption and repopulation could be implicated in the transmission and dissemination of this parasite across the Mexican Pacific coast. The aim of this study was two-fold. First, we evaluated the P. marinus infection parameters by PCR and RFTM (Ray’s fluid thioglycollate medium) in C. virginica from four major lagoons (Términos Lagoon, Campeche; Carmen-Pajonal-Machona Lagoon complex, Tabasco; Mandinga Lagoon, Veracruz; and La Pesca Lagoon, Tamaulipas) from the Gulf of Mexico. Secondly, we used DNA sequence analyses of the ribosomal non-transcribed spacer (rNTS) region of P. marinus to determine the possible translocation of this species from the Gulf of Mexico to the Mexican Pacific coast.Results Perkinsus marinus prevalence by PCR was 57.7% (338 out of 586 oysters) and 38.2% (224 out of 586 oysters) by RFTM. The highest prevalence was observed in the Carmen-Pajonal-Machona Lagoon complex in the state of Tabasco (73% by PCR and 58% by RFTM) and the estimated weighted prevalence (WP) was less than 1.0 in the four lagoons. Ten unique rDNA-NTS sequences of P. marinus [termed herein the “P. marinus (Pm) haplotype”] were identified in the Gulf of Mexico sample. They shared 96–100% similarity with 18 rDNA-NTS sequences from the GenBank database which were derived from 16 Mexican Pacific coast infections and two sequences from the USA. The phylogenetic tree and the haplotype network showed that the P. marinus rDNA-NTS sequences from Mexico were distant from the rDNA-NTS sequences of P. marinus reported from the USA. The ten rDNA-NTS sequences described herein were restricted to specific locations displaying different geographical connections within the Gulf of Mexico; the Carmen-Pajonal-Machona Pm1 haplotype from the state of Tabasco shared a cluster with P. marinus isolates reported from the Mexican Pacific coast.ConclusionsThe rDNA-NTS sequences of P. marinus from the state of Tabasco shared high similarity with the reference rDNA-NTS sequences from the Mexican Pacific coast. The high similarity suggests a transfer of oysters infected with P. marinus from the Mexican part of the Gulf of Mexico into the Mexican Pacific coast.

Detection of haplosporidian protistan parasites supports an increase to their known diversity, geographic range and bivalve host specificity

“…for aquaculture) and unintentionally (i.e. as stowaways in ship ballast water or on hulls), brings the threat of ‘pathogen spillover’ into introduced areas and highly-susceptible host populations (Carnegie et al ., 2016; Ek-Huchim et al ., 2017). It is also recognized that coastal development may unbalance marine parasite-host systems (Coen and Bishop, 2015), as past emergent and resurgent diseases in wildlife appear to be associated with anthropogenic activities (Harvell et al ., 1999; Daszak et al ., 2000).…”

“…Haplosporidium nelsoni, the causative agent of MSX disease in the eastern oyster Crassostrea virginica in North America, was detected for the first time in Irish and Spanish Pacific oysters Crassostrea gigas and in O. edulis in Ireland (Lynch et al, 2013). In addition, Minchinia mercenariae, reported to cause infections in the hard clam Mercenaria mercenaria from the Atlantic coast of the United States (Ford et al, 2009), was detected in the common cockle Cerastoderma edule in the Netherlands (Engelsma et al, 2014) and the UK (Longshaw and Malham, 2013) where it was implicated in host population crashes, and an M. mercenariae-like parasite was recently confirmed in C. edule in Galicia, Spain (Ramilo et al, 2017).…”

A qPCR-Based Survey of Haplosporidium nelsoni and Perkinsus spp. in the Eastern Oyster, Crassostrea virginica in Maine, USA

“…Alternatively, the translocation of P. chesapeaki strains from other sites may explain the higher qPCR-prevalence values. Translocation of P. marinus between the Gulf of Mexico and the Pacific Ocean has been described based on genetic studies [49]. Still without an exhaustive genetic analysis of P. marinus and P. chesapeaki isolated from Maine oysters, translocation cannot be ruled out as an explanation for recently higher qPCR-prevalence values in Maine.…”

Detection of Perkinsus marinus in a wild population of the horsemussel Modiolus capax from the southwestern Gulf of California

“…Entre los parásitos más importantes que se han reportado en moluscos bivalvos del Golfo de California destacan el virus OsHV-1 y los protozoarios Marteilia refringens (Grizel, Comps, Bonami, Cousserans, Duthoit & Le Pennec, 1974) y Perkinsus marinus [(Mackin, Owen & Collier) Levine, 1978], los cuales, han sido encontrados en las almejas Ruditapes philippinarum (Adams & Reeve, 1850) (Renault et al, 2001) y Scapharca broughtonii (Adams & Reeve, 1850) (Xin et al, 2018), y en los ostiones Magallana (≈Crassostrea) gigas (Thunberg, 1973) y Crassostrea corteziensis (Hertlein, 1951) (Cáceres-Martínez et al, 2008Grijalva-Chon et al, 2013Enríquez-Espinoza et al, 2015). Específicamente para P. marinus, desde que se comprobó su transfaunación de las costas del Océano Atlántico (Bushek & Allen, 1996;Reece et al, 2008;Cáceres-Martínez et al, 2016) y, posteriormente, se confirmó su presencia en las costas del Pacífico Mexicano (Cáceres-Martínez et al, 2008;Ek-Huchim et al, 2017), este protozoario ha sido detectado en ostiones cultivados, fuera (Cáceres-Martínez et al, 2008) y dentro (Cáceres-Martínez et al, 2018) del Golfo de California, sin afectar su producción (Villanueva-Fonseca & Escobedo-Bonilla, 2013;Martínez-García et al, 2017;Villanueva-Fonseca et al, 2020); aunque también, se ha reportado asociado a mortalidades de ostreidos (Enríquez-Espinoza et al, 2010). Debido a la fácil dispersión de este parásito y el riesgo que implica su potencial de infección en otras especies de moluscos (Villalba et al, 2004), el Laboratorio de Malacología del Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional (CII-DIR-Unidad Sinaloa) del Instituto Politécnico Nacional (IPN), desde hace una década, realiza un registro de la ocurrencia de P. marinus y organismos parecidos a Perkinsus spp., en diferentes especies de bivalvos de poblaciones silvestres y cultivadas que habitan en algunas lagunas de la costa sureste del Golfo de California.…”