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California mussels (Mytilus californianus) as sentinels for marine contamination with Sarcocystis neurona

Published online by Cambridge University Press:  22 March 2016

LAUREN MICHAELS ,
DANIEL REJMANEK ,
BEATRIZ AGUILAR ,
PATRICIA CONRAD  and
KAREN SHAPIRO Open the ORCID record for KAREN SHAPIRO [Opens in a new window]
LAUREN MICHAELS
Affiliation:
Pathology, Microbiology and Immunology Department, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA
DANIEL REJMANEK
Affiliation:
Center for Animal Health and Food Safety, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA
BEATRIZ AGUILAR
Affiliation:
Pathology, Microbiology and Immunology Department, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA
PATRICIA CONRAD
Affiliation:
Pathology, Microbiology and Immunology Department, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA One Health Institute, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA
KAREN SHAPIRO*
Affiliation:
Pathology, Microbiology and Immunology Department, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA One Health Institute, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA
*
*Corresponding author. Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, 4206 VM3A, One Shields Avenue, Davis, CA 95616, USA or One Health Institute, School of Veterinary Medicine, University of California Davis, One Shields Avenue, Davis, CA 95616, USA. Phone: +001 519-546-0324. Fax: +001 530-752-3349. E-mail: kshapiro@ucdavis.edu
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Summary

Sarcocystis neurona is a terrestrial parasite that can cause fatal encephalitis in the endangered Southern sea otter (Enhydra lutris nereis). To date, neither risk factors associated with marine contamination nor the route of S. neurona infection to marine mammals has been described. This study evaluated coastal S. neurona contamination using California mussels (Mytilus californianus) as sentinels for pathogen pollution. A field investigation was designed to test the hypotheses that (1) mussels can serve as sentinels for S. neurona contamination, and (2) S. neurona contamination in mussels would be highest during the rainy season and in mussels collected near freshwater. Initial validation of molecular assays through sporocyst spiking experiments revealed the ITS-1500 assay to be most sensitive for detection of S. neurona, consistently yielding parasite amplification at concentrations ⩾5 sporocysts/1 mL mussel haemolymph. Assays were then applied on 959 wild-caught mussels, with detection of S. neurona confirmed using sequence analysis in three mussels. Validated molecular assays for S. neurona detection in mussels provide a novel toolset for investigating marine contamination with this parasite, while confirmation of S. neurona in wild mussels suggests that uptake by invertebrates may serve as a route of transmission to susceptible marine animals.

Keywords

Sarcocystis neuronaCalifornia mussels (Mytilus californianus)HaemolymphDetectionMarineSporocystsSea otters (Enhydra lutris nereis)
Type
Research Article
Information
Parasitology , Volume 143 , Issue 6 , May 2016 , pp. 762 - 769
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Arkush, K. D., Miller, M. A., Leutenegger, C. M., Gardner, I. A., Packham, A. E., Heckeroth, A. R., Tenter, A. M., Barr, B. C. and Conrad, P. A. (2003). Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). International Journal for Parasitology, 33, 1087–1097.Google Scholar
Asmundsson, I. M. and Rosenthal, B. M. (2006). Isolation and characterization of microsatellite markers from Sarcocystis neurona, a causative agent of equine protozoal myeloencephalitis. Molecular Ecology Notes 6, 8–10.Google Scholar
Barbosa, L., Johnson, C. K., Lambourn, D. M., Gibson, A. K., Haman, K. H., Huggins, J. L., Sweeny, A. R., Sundar, N., Raverty, S. A. and Grigg, M. E. (2015). A novel Sarcocystis neurona genotype XIII is associated with severe encephalitis in an unexpectedly broad range of marine mammals from the northeastern Pacific Ocean. International Journal for Parasitology 45, 595–603.Google Scholar
Carlson-Bremer, D. P., Gulland, F. M. D., Johnson, C. K., Colegrove, K. M. and Van Bonn, W. G. (2012). Diagnosis and treatment of Sarcocystis neurona-induced myositis in a free-ranging California sea lion. JAVMA – Journal of the American Veterinary Medical Association 240, 324–328.CrossRefGoogle Scholar
Conrad, P. A., Miller, M. A., Kreuder, C., James, E. R., Mazet, J., Dabritz, H., Jessup, D. A., Gulland, F. and Grigg, M. E. (2005). Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal for Parasitology 35, 1155–1168.Google Scholar
Dubey, J. P., Miller, N. L. and Frenkel, J. K. (1970). Characterization of new fecal form of Toxoplasma gondii . Journal of Parasitology 56, 447–&.Google Scholar
Dubey, J. P., Davis, S. W., Speer, C. A., Bowman, D. D., Delahunta, A., Granstrom, D. E., Topper, M. J., Hamir, A. N., Cummings, J. F. and Suter, M. M. (1991). Sarcocystis neurona n. sp. (Protozoa, Apicomplexa), the etiologic agent of equine protozoal myeloencephalitis. Journal of Parasitology 77, 212–218.CrossRefGoogle Scholar
Dubey, J. P., Lindsay, D. S., Kerber, C. E., Kasai, N., Pena, H. F. J., Gennari, S. M., Kwok, O. C. H., Shen, S. K. and Rosenthal, B. M. (2001 a). First isolation of Sarcocystis neurona from the South American opossum, Didelphis albiventris, from Brazil. Veterinary Parasitology 95, 295–304.Google Scholar
Dubey, J. P., Lindsay, D. S., Saville, W. J. A., Reed, S. M., Granstrom, D. E. and Speer, C. A. (2001 b). A review of Sarcocystis neurona and equine protozoal myeloencephalitis (EPM). Veterinary Parasitology 95, 89–131.Google Scholar
Dubey, J. P., Rosypal, A. C., Rosenthal, B. M., Thomas, N. J., Lindsay, D. S., Stanek, J. F., Reed, S. M. and Saville, W. J. A. (2001 c). Sarcocystis neurona infections in sea otter (Enhydra lutris): evidence for natural infections with sarcocysts and transmission of infection to opossums (Didelphis virginiana). Journal of Parasitology 87, 1387–1393.Google Scholar
Dubey, J. P., Howe, D. K., Furr, M., Saville, W. J., Marsh, A. E., Reed, S. M. and Grigg, M. E. (2015). An update on Sarcocystis neurona infections in animals and equine protozoal myeloencephalitis (EPM). Veterinary Parasitology 209, 1–42.Google Scholar
Dubey, J. P., Saville, W. J., Sreekumar, C., Shen, S. K., Lindsay, D. S., Pena, H. F., Vianna, M. C., Gennari, S. M. and Reed, S. M. (2002). Effects of high temperature and disinfectants on the viability of Sarcocystis neurona sporocysts. Journal of Parasitology 88, 1252–1254.Google Scholar
Fenger, C. K. (1997). Equine protozoal myeloencephalitis. Compendium on Continuing Education for the Practicing Veterinarian 19, 513–523.Google Scholar
Fenger, C. K., Granstrom, D. E., Langemeier, J. L., Stamper, S., Donahue, J. M., Patterson, J. S., Gajadhar, A. A., Marteniuk, J. V., Zhou, X. M. and Dubey, J. P. (1995). Identification of opossums (Didelphis virginiana) as the putative definitive host of Sarcocystis neurona . Journal of Parasitology 81, 916–919.Google Scholar
Gibson, A. K., Raverty, S., Lambourn, D. M., Huggins, J., Magargal, S. L. and Grigg, M. E. (2011). Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species. PLoS Neglected Tropical Diseases 5, e1142. doi: 10.1371/journal.pntd.0001142.Google Scholar
Hutchison, W. M., Dunachie, J. F., Siim, J. C. and Works, K. (1970). Coccidian like nature of Toxoplasma gondii . British Medical Journal 1, 142–144.Google Scholar
Johnson, C. K., Tinker, M. T., Estes, J. A., Conrad, P. A., Staedler, M., Miller, M. A., Jessup, D. A. and Mazet, J. A. K. (2009). Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system. Proceedings of the National Academy of Sciences of the United States of America 106, 2242–2247.Google Scholar
Kreuder, C., Miller, M. A., Jessup, D. A., Lowenstein, L. J., Harris, M. D., Ames, J. A., Carpenter, T. E., Conrad, P. A. and Mazet, J. A. K. (2003). Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998–2001. Journal of Wildlife Diseases 39, 495–509.Google Scholar
Lapointe, J. M., Duignan, P. J., Marsh, A. E., Gulland, F. M., Barr, B. C., Naydan, D. K., King, D. P., Farman, C. A., Huntingdon, K. A. B. and Lowenstine, L. J. (1998). Meningoencephalitis due to a Sarcocystis neurona-like protozoan in Pacific harbor seals (Phoca vitulina richardsi). Journal of Parasitology 84, 1184–1189.Google Scholar
Marsh, A. E., Barr, B. C., Tell, L., Bowman, D. D., Conrad, P. A., Ketcherside, C. and Green, T. (1999). Comparison of the internal transcribed spacer, ITS-1, from Sarcocystis falcatula isolates and Sarcocystis neurona . Journal of Parasitology 85, 750–757.Google Scholar
Miller, M. A., Sverlow, K., Crosbie, P. R., Barr, B. C., Lowenstine, L. J., Gulland, F. M., Packham, A. and Conrad, P. A. (2001). Isolation and characterization of two parasitic protozoa from a Pacific harbor seal (Phoca vitulina richardsi) with meningoencephalomyelitis. Journal of Parasitology 87, 816–822.CrossRefGoogle ScholarPubMed
Miller, M. A., Gardner, I. A., Kreuder, C., Paradies, D. M., Worcester, K. R., Jessup, D. A., Dodd, E., Harris, M. D., Ames, J. A., Packham, A. E. and Conrad, P. A. (2002). Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). International Journal for Parasitology 32, 997–1006.Google Scholar
Miller, M. A., Grigg, M. E., Kreuder, C., James, E. R., Melli, A. C., Crosbie, P. R., Jessup, D. A., Boothroyd, J. C., Brownstein, D. and Conrad, P. A. (2004). An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and is a cause of mortality. International Journal for Parasitology 34, 275–284.Google Scholar
Miller, W. A., Miller, M. A., Gardner, I. A., Atwill, E. R., Harris, M., Ames, J., Jessup, D., Melli, A., Paradies, D., Worcester, K., Olin, P., Barnes, N. and Conrad, P. A. (2005). New genotypes and factors associated with Cryptosporidium detection in mussels (Mytilus spp.) along the California coast. International Journal for Parasitology 35, 1103–1113.CrossRefGoogle ScholarPubMed
Miller, M. A., Barr, B. C., Nordhausen, R., James, E. R., Magargal, S. L., Murray, M., Conrad, P. A., Toy-Choutka, S., Jessup, D. A. and Grigg, M. E. (2009). Ultrastructural and molecular confirmation of the development of Sarcocystis neurona tissue cysts in the central nervous system of southern sea otters (Enhydra lutris nereis). International Journal for Parasitology 39, 1363–1372.Google Scholar
Miller, M. A., Conrad, P. A., Harris, M., Hatfield, B., Langlois, G., Jessup, D. A., Magargal, S. L., Packham, A. E., Toy-Choutka, S., Melli, A. C., Murray, M. A., Gulland, F. M. and Grigg, M. E. (2010). A protozoal-associated epizootic impacting marine wildlife: Mass-mortality of southern sea otters (Enhydra lutris nereis) due to Sarcocystis neurona infection. Veterinary Parasitology 172, 183–194.Google Scholar
Rejmanek, D., Vanwormer, E., Miller, M. A., Mazet, J. A. K., Nichelason, A. E., Melli, A. C., Packham, A. E., Jessup, D. A. and Conrad, P. A. (2009). Prevalence and risk factors associated with Sarcocystis neurona infections in opossums (Didelphis virginiana) from central California. Veterinary Parasitology 166, 8–14.Google Scholar
Rejmanek, D., Miller, M. A., Grigg, M. E., Crosbie, P. R. and Conrad, P. A. (2010). Molecular characterization of Sarcocystis neurona strains from opossums (Didelphis virginiana) and intermediate hosts from Central California. Veterinary Parasitology 170, 20–29.Google Scholar
Renault, T., Le Deuff, R. M., Lipart, C. and Delsert, C. (2000). Development of a PCR procedure for the detection of a herpes-like virus infecting oysters in France. Journal of Virological Methods 88, 41–50.Google Scholar
Shapiro, K., Mazet, J. A. K., Schriewer, A., Wuertz, S., Fritz, H., Miller, W. A., Largier, J. and Conrad, P. A. (2010). Detection of Toxoplasma gondii oocysts and surrogate microspheres in water using ultrafiltration and capsule filtration. Water Research 44, 893–903.CrossRefGoogle ScholarPubMed
Shapiro, K., Miller, M. and Mazet, J. (2012). Temporal association between land-based runoff events and California sea otter (Enhydra lutris nereis) Protozoal Mortalities. Journal of Wildlife Diseases 48, 394–404.CrossRefGoogle ScholarPubMed
Shapiro, K., VanWormer, E., Aguilar, B. and Conrad, P. A. (2015). Surveillance for Toxoplasma gondii in California mussels (Mytilus californianus) reveals transmission of atypical genotypes from land to sea. Environmental Microbiology 17, 4177–4188.Google Scholar
Staggs, S. E., Keely, S. P., Ware, M. W., Schable, N., See, M. J., Gregorio, D., Zou, X., Su, C., Dubey, J. P. and Villegas, E. N. (2015). The development and implementation of a method using blue mussels (Mytilus spp.) as biosentinels of Cryptosporidium spp. and Toxoplasma gondii contamination in marine aquatic environments. Parasitology Research 114, 4655–4667.Google Scholar
Tanhauser, S. M., Yowell, C. A., Cutler, T. J., Greiner, E. C., MacKay, R. J. and Dame, J. B. (1999). Multiple DNA markers differentiate Sarcocystis neurona and Sarcocystis falcatula . Journal of Parasitology 85, 221–228.Google Scholar
Thomas, N. J., Dubey, J. P., Lindsay, D. S., Cole, R. A. and Meteyer, C. U. (2007). Protozoal meningoencephalitis in sea otters (Enhydra lutris): a histopathological and immunohistochemical study of naturally occurring cases. Journal of Comparative Pathology 137, 102–121.CrossRefGoogle ScholarPubMed
Villena, I., Aubert, D., Gomis, P., Ferte, H., Inglard, J. C., Denis-Bisiaux, H., Dondon, J. M., Pisano, E., Ortis, N. and Pinon, J. M. (2004). Evaluation of a strategy for Toxoplasma gondii oocyst detection in water. Applied and Environmental Microbiology 70, 4035–4039.Google Scholar
Wendte, J. M., Miller, M. A., Nandra, A. K., Peat, S. M., Crosbie, P. R., Conrad, P. A. and Grigg, M. E. (2010). Limited genetic diversity among Sarcocystis neurona strains infecting southern sea otters precludes distinction between marine and terrestrial isolates. Veterinary Parasitology 169, 37–44.Google Scholar