Newly detected, virulent Toxoplasma gondii COUG strain causing fatal steatitis and toxoplasmosis in southern sea otters (Enhydra lutris nereis)

Abstract

From February 2020 to March 2022, four southern sea otters (Enhydra lutris nereis) stranded in California with severe protozoal steatitis and systemic toxoplasmosis. Three of the infected otters stranded within 26 km of each other, and all four animals died during periods of increased rainfall-driven surface water runoff. High parasite burdens were observed in all tissues except the central nervous system, and toxoplasmosis with severe protozoal steatitis was the primary cause of death for all cases. This lesion pattern differs substantially from all prior reports of toxoplasmosis in sea otters. All cases were T. gondii-positive via serology, immunohistochemistry, and PCR. Multilocus sequence typing at 13 loci revealed that all were infected with the same strain of T. gondii, previously characterized as an atypical and rare genotype in North America (TgCgCa1, or COUG). The COUG genotype was first isolated from mountain lions in British Columbia, Canada during investigation of a waterborne outbreak of toxoplasmosis in humans. This genotype has not been previously reported from sea otters, nor any aquatic species. All prior T. gondii strains obtained from >140 southern sea otters represent Type II or Type X strains, or variants of these genotypes. Archival necropsy data (>1,000 animals over 24 years) were negative for prior cases of severe T. gondii-associated steatitis prior to the cases described herein, and no sublethal COUG T. gondii infections have been previously indentified in sea otters. According to prior studies, the T. gondii COUG genotype is highly virulent in mice and is unusual among T. gondii isolates in eliciting a Type I interferon response in murine and human cells in vitro; this unusual immunomodulatory response could explain the apparent high virulence of this atypical T. gondii strain. Our findings reveal a novel and concerning lesion pattern for sea otters with toxoplasmosis. Due to high zoonotic potential and the risk of infection via shared marine food resources, these findings may also indicate potential health threats for other animals and humans.

High prevalence and diversity of Toxoplasma gondii DNA in feral cat feces from coastal California

“…Finding Type X and X variant T. gondii DNA in feces suggests that free-ranging feral cats are exposed to non-archetypal T. gondii strains, most likely in prey, that can result in shedding of more virulent T. gondii oocysts, which was previously documented among owned domestic cats [16,55]. A newly described virulent genotype for sea otters in California, COUG, has a Type I allele at the B1 locus, which was the dominant B1 allele in our feral cat fecal samples [56]. We were unable to further characterize T. gondii in feral cat feces due to low quality/quantity of DNA, so presence of the COUG genotype has not been confirmed in feral cats at this time.…”

Toxoplasma gondii Me49 and NED strains arrest host cell cycle progression and alter chromosome segregation in a strain-independent manner

“…To our best knowledge, available data on T. gondii -driven host cell cycle modulation currently refer to haplotype I tachyzoites (RH strain) and indicate that this clonal lineage might control host cell cycle progression to ease its intracellular asexual development ( Brunet et al, 2008 ; Molestina et al, 2008 ; Velásquez et al, 2019 ; Wong et al, 2020 ; Pierre-Louis et al, 2022 ). Since several typical and atypical clonal lineages of T. gondii occur worldwide and show variable pathogenicity ( Dardé et al, 2014 ; Miller et al, 2023 ), we aimed to compare recent RH data (haplotype I) ( Velásquez et al, 2019 ) with haplotypes II and III (Me49 and NED, respectively) by infecting the same host cell type. In our hands, the replication times of the ME49 and NED strains in BUVEC proved comparable to those of the RH strain, allowing us to use this primary cell culture system for comparative approaches.…”

A parasite odyssey: An RNA virus concealed in Toxoplasma gondii

“…2003 ). A recent report of COUGAR strain infection in four southern sea otters ( Enhydra lutris nereis ) observed severe myocarditis and marked subcutaneous and peritoneal steatitis ( Miller et al. 2023 ).…”