Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: New linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters

California Department of Fish and Game, Marine Wildlife Veterinary Care and Research Center, Santa Cruz, CA 95060, United States.
International Journal for Parasitology (Impact Factor: 3.87). 03/2008; 38(11):1319-28. DOI: 10.1016/j.ijpara.2008.02.005
Source: PubMed


Sea otters in California are commonly infected with Toxoplasma gondii. A unique Type X strain is responsible for 72% of otter infections, but its prevalence in terrestrial animals and marine invertebrates inhabiting the same area was unknown. Between 2000 and 2005, 45 terrestrial carnivores (lions, bobcats, domestic cats and foxes) and 1396 invertebrates (mussels, clams and worms) were screened for T. gondii using PCR and DNA sequencing to determine the phylogeographic distribution of T. gondii archetypal I, II, III and Type X genotypes. Marine bivalves have been shown to concentrate T. gondii oocysts in the laboratory, but a comprehensive survey of wild invertebrates has not been reported. A California mussel from an estuary draining into Monterey Bay was confirmed positive for Type X T. gondii by multilocus PCR and DNA sequencing at the B1 and SAG1 loci. This mussel was collected from nearshore marine waters just after the first significant rainfall event in the fall of 2002. Of 45 carnivores tested at the B1, SAG1, and GRA6 typing loci, 15 had PCR-confirmed T. gondii infection; 11 possessed alleles consistent with infection by archetypal Type I, II or III strains and 4 possessed alleles consistent with Type X T. gondii infection. No non-canonical alleles were identified. The four T. gondii strains with Type X alleles were identified from two mountain lions, a bobcat and a fox residing in coastal watersheds adjacent to sea otter habitat near Monterey Bay and Estero Bay. Confirmation of Type X T. gondii in coastal-dwelling felids, canids, a marine bivalve and nearshore-dwelling sea otters supports the hypotheses that feline faecal contamination is flowing from land to sea through surface runoff, and that otters can be infected with T. gondii via consumption of filter-feeding marine invertebrates.

Download full-text


Available from: Andrea E Packham, Oct 06, 2015
74 Reads
  • Source
    • "In aquatic environments, T. gondii is found in a large variety of marine mammals in California, which is surprising since marine mammals do not consume intermediate hosts. To evaluate how these organisms were infected, Miller et al. (2008) tested tissues collected from various animals along the California coast (terrestrial and marine wildlife and marine and estuarine invertebrates). They found that terrestrial carnivores and wild mussels were infected by the same strain of T. gondii (type X). "
    Environmental Science and Pollution Research 03/2015; · 2.83 Impact Factor
  • Source
    • "In the present study using the harbour seal as an animal model for pinnipeds and other closely related marine mammals, we therefore investigated the formation of ETs by PMN and monocytes against the pathogenic apicomplexan protozoa T. gondii. This parasite is a facultative heteroxenous, polyxenous protozoa which possess the capability to infect virtually all warm-blooded animals, including marine mammals (Dubey et al., 2011; Tenter et al., 2000), such as seals (Cabezón et al., 2011; Fujii et al., 2007; Simon et al., 2011), sea otter (Conrad et al., 2005; Goldstein et al., 2011; Miller et al., 2008), dolphins (Dubey et al., 2008) and whales (Mazzariol et al., 2012). To our best knowledge, we here report for the first time on T. gondiitriggered ET formation in harbour seal-PMN and -monocytes. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Extracellular traps (ETs) are composed of nuclear DNA as backbone adorned with histones, cytoplasmic antimicrobial peptides/proteins which are released from a range of vertebrate and invertebrate host immune cells in response to several invading pathogens. Until now this ancient novel innate defence mechanism has not been demonstrated in any marine mammal. Interactions of harbour seal (Phoca vitulina)-PMN and -monocytes with viable tachyzoites of Toxoplasma gondii were investigated in this respect in vitro. For the demonstration and quantification of harbour seal PMN- and monocyte-derived ETs, extracellular DNA was stained with Sytox Orange. Fluorescence assays as well as scanning electron microscopy (SEM) analyses demonstrated PMN- and monocyte-promoted ET formation rapidly being induced upon contact with T. gondii-tachyzoites. The co-localization of extracellular DNA decorated with histones (H3), neutrophil elastase (NE) and myeloperoxidase (MPO) in parasite entrapping structures confirmed the classical characteristics of PMN- and monocyte-promoted ETs. Exposure of harbour seal PMN and monocytes to viable tachyzoites resulted in a significant induction of ETs when compared to negative controls. Harbour seal-ETs were efficiently abolished by DNase I treatment and were reduced after PMN and monocytes pre-incubation with the NADPH oxidase inhibitor diphenilane iodondium. Tachyzoites of T. gondii were firmly entrapped and immobilized within harbour seal-ETs structures. To our best knowledge, we here report for the first time on T. gondii-induced ET formation in harbour seal-PMN and -monocytes. Our results strongly indicate that PMN- and monocyte-triggered ETs represent a relevant and ancient conserved effector mechanism of the pinniped innate immune system as reaction against the pathogenic protozoon T. gondii and probably against other foreign pathogens occurring in the ocean environment. Copyright © 2015. Published by Elsevier Ltd.
    Developmental & Comparative Immunology 02/2015; 50(2). DOI:10.1016/j.dci.2015.02.002 · 2.82 Impact Factor
  • Source
    • "In natural conditions, T. gondii has been molecularly detected in Mytilus californianus, a wild mussel in the USA (Miller et al., 2008), in edible marketed shellfish in Brazil (Esmerini et al., 2010), and more recently in farmed shellfish in Italy (Putignani et al., 2011). Cyclospora has been identified by staining in Caelatura Iaronia pruneri from markets in Alexandria (Egypt) (Negm, 2003). "
    [Show abstract] [Hide abstract]
    ABSTRACT: To evaluate the presence of Toxoplasma gondii and Cyclospora cayetanensis in edible shellfish, a total of 795 specimens of Mytilus galloprovincialis from 8 different sites on the west coast of Turkey (Bays of Izmir and Mersin) were examined. Fifty-three pooled samples were created and subjected to EvaGreen® RealTime PCR assay and HRM analysis for protozoans detection and oocyst quantification. Seven out of 8 sites were contaminated with at least one protozoan species. Twenty-one out of 53 (39.6%) samples tested positive for T. gondii, C. cayetanensis or both pathogens: 26.4% samples positive for C. cayetanensis; 9.4% for T. gondii, and 3.8% for both protozoans. The number of oocysts in positive samples ranged from 6 to 30 for T. gondii and from 3 to 48 for C. cayetanensis. This is the first report of T. gondii Type 1, and C. cayetanensis in M. galloprovincialis, the most consumed shellfish species in Turkey.
    Food Microbiology 12/2014; 44:128–135. DOI:10.1016/ · 3.33 Impact Factor
Show more