Aquatic polymers can drive pathogen transmission in coastal ecosystems

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1795, 2014, Pages

  Shapiro, Karen ^a   Krusor, Colin ^a   Mazzillo, Fernanda F M ^c   Conrad, Patricia A ^a   Largier, John L ^b   Mazet, Jonna A K ^a   Silver, Mary W ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA DAVIS   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Extracellular polymeric substances; Marine transmission; Sea otter; Toxoplasma gondii; Transparent exopolymer particles; Zoonotic pathogen

Indexed keywords

AGGREGATION; BIOFILM; BROWN ALGA; COASTAL ZONE; FOOD WEB; HABITAT TYPE; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; MACROALGA; POLYMER;

ENHYDRA; TOXOPLASMA GONDII;

PARTICULATE MATTER; POLYMER;

ANALYSIS; ANIMAL; ANIMAL TOXOPLASMOSIS; CALIFORNIA; FOOD CHAIN; KELP; OTTER; PARASITOLOGY; PARTICULATE MATTER; PHYSIOLOGY; SNAIL; TOXOPLASMA; TRANSMISSION;

ANIMALS; CALIFORNIA; FOOD CHAIN; KELP; OTTERS; PARTICULATE MATTER; POLYMERS; SNAILS; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

EID: 84908146241     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1287     Document Type: Article

References (49)

1. Moore MN et al. 2013 Oceans and human health (OHH): a European perspective from the Marine Board of the European Science Foundation (Marine Board-ESF). Microb. Ecol. 65, 889-900. (doi:10. 1007/s00248-013-0204-5)
2. Verdugo P, Alldredge AL, Azam F, Kirchman DL, Passow U, Santschi PH. 2004 The oceanic gel phase: a bridge in the DOM-POM continuum. Mar. Chem. 92, 67-85. (doi:10.1016/j.marchem. 2004.06.017)
3. Wotton RS. 2004 The essential role of exopolymers (EPS) in aquatic systems. In Oceanography and marine biology: an annual review, vol. 42 (eds RN Gibson, RJA Atkinson, JDM Gordon), pp. 57-94. Boca Raton, FL: CRC Press.
4. Dubey JP, Beattie CP. 1988 Toxoplasmosis of animals and man. Boca Raton, FL: CRC Press.
5. Hutchison WM, Dunachie JF, Siim JC, Work K. 1969 Life cycle of Toxoplasma gondii. Br. Med. J. 4, 806. (doi:10.1136/bmj.4.5686.806-b)
6. Dumetre A, Darde ML. 2003 How to detect Toxoplasma gondii oocysts in environmental samples? FEMS Microbiol. Rev. 27, 651-661. (doi:10.1016/S0168-6445(03)00071-8)
7. Miller MA. 2008 Tissue cyst-forming coccidia of marine mammals. In Zoo and wild animal medicine (eds M Fowler, R Miller), pp. 319-340. St Louis, MO: Sounders Elsevier.
8. Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, Dabritz H, Jessup DA, Gulland F, Grigg ME. 2005 Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int. J. Parasitol. 35, 1155-1168. (doi:10.1016/j.ijpara.2005.07.002)
9. Jones JL, Dargelas V, Roberts J, Press C, Remington JS, Montoya JG. 2009 Risk factors for Toxoplasma gondii infection in the United States. Clin. Infect. Dis. 49, 878-884. (doi:10.1086/605433)
10. Johnson CK, Tinker MT, Estes JA, Conrad PA, Staedler M, Miller MA, Jessup DA, Mazet JA. 2009 Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system. Proc. Natl Acad. Sci. USA 106, 2242-2247. (doi:10.1073/ pnas.0806449106)
11. Alldredge AL, Passow U, Logan BE. 1993 The abundance and significance of a class of large, transparent organic particles in the ocean. Deep-Sea Res. Part I-Oceanogr. Res. Pap. 40, 1131-1140. (doi:10.1016/0967-0637(93)90129-q)
12. Silver MW, Shanks AL, Trent JD. 1978 Marine snow-microplankton habitat and source of small-scale patchiness in pelagic populations. Science 201, 371-373. (doi:10.1126/science.201. 4353.371)
13. Alldredge AL, Silver MW. 1988 Characteristics, dynamics and significance of marine snow. Progr. Oceanogr. 20, 41-82. (doi:10.1016/0079- 6611(88)90053-5)
14. Burd AB, Jackson GA. 2009 Particle aggregation. Annu. Rev. Mar. Sci. 1, 65-90. (doi:10.1146/ annurev.marine.010908.163904)
15. Passow U. 2002 Transparent exopolymer particles (TEP) in aquatic environments. Progr. Oceanogr. 55, 287-333. (doi:10.1016/S0079- 6611(02)00138-6)
16. Lyons MM, Ward JE, Smolowitz R, Uhlinger KR, Gast RJ. 2005 Lethal marine snow: pathogen of bivalve mollusc concealed in marine aggregates. Limnol. Oceanogr. 50, 1983-1988. (doi:10.4319/lo.2005. 50.6.1983)
17. Lyons M, Lau Y, Carden W, Ward J, Roberts S, Smolowitz R, Vallino J, Allam B. 2007 Characteristics of marine aggregates in shallow-water ecosystems: implications for disease ecology. Ecohealth 4, 406-420. (doi:10.1007/s10393-007-0134-0)
18. Shapiro K, Miller WA, Silver MW, Odagiri O, Largier JL, Conrad PA, Mazet JAK. 2012 Association of zoonotic pathogens with fresh, estuarine, and marine macroaggregates. Microb. Ecol. 64, 928-933. (doi:10.1007/s00248-012-0147-2)
19. Shapiro K, Silver MW, Largier J, Conrad PA, Mazet JAK. 2012 Association of Toxoplasma gondii oocysts with fresh, estuarine, and marine macroaggregates. Limnol. Oceanogr. 57, 449-456. (doi:10.4319/lo. 2012.57.2.0449)
20. Ward JE, Kach DJ. 2009 Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar. Environ. Res. 68, 137-142. (doi:10. 1016/j.marenvres.2009.05.002)
21. Passow U, Alldredge AL, Logan BE. 1994 The role of particulare carbohydrate exudates in the flocculation of diatom blooms. Deep-Sea Res. Part I-Oceanogr. Res. Pap. 41, 335-357. (doi:10.1016/0967-0637 (94)90007-8)
22. Mazzillo FFM, Shapiro K, Silver MW. 2013 A new pathogen transmission mechanism in the ocean: the case of sea otter exposure to the land-parasite Toxoplasma gondii. PLoS ONE 8, e82477. (doi:10. 1371/journal.pone.0082477)
23. Krusor C. 2012 Acquisition, concentration, and retention of Toxoplasma gondii oocysts from seawater by marine snails. Proquest, UMI Dissertations Publishing, University of California, Davis, CA, USA.
24. Passow U, Alldredge AL. 1995 A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol. Oceanogr. 40, 1326-1335. (doi:10.4319/lo.1995. 40.7.1326)
25. Utermohl H. 1958 Zur Vervollkommnung der quantitativen Phytoplanktonmethodik. Mitt In Ver Limnol. 9, 1-38.
26. Fritz H, Barr B, Packham A, Melli A, Conrad PA. 2012 Methods to produce and safely work with large numbers of Toxoplasma gondii oocysts and bradyzoite cysts. J. Microbiol. Methods 88, 47-52. (doi:10.1016/j.mimet.2011.10.010)
27. Shapiro K, Largier J, Mazet JAK, Bernt W, Ell JR, Melli AC, Conrad PA. 2009 Surface properties of Toxoplasma gondii oocysts and surrogate microspheres. Appl. Environ. Microbiol. 75, 1185-1191. (doi:10.1128/Aem.02109-08)
28. Shanks AL, Edmondson EW. 1989 Laboratory-made artificial marine snow-a biological model of the real thing. Mar. Biol. 101, 463-470. (doi:10.1007/ BF00541648)
29. Lyons MM, Ward JE, Gaff H, Hicks RE, Drake JM, Dobbs FC. 2010 Theory of island biogeography on a microscopic scale: organic aggregates as islands for aquatic pathogens. Aquat. Microb. Ecol. 60, 1-13. (doi:10.3354/ame01417)
30. Shapiro K, Mazet JAK, Schriewer A, Wuertz S, Fritz H, Miller WA, Largier J, Conrad PA. 2010 Detection of Toxoplasma gondii oocysts and surrogate microspheres in water using ultrafiltration and capsule filtration. Water Res. 44, 893-903. (doi:10. 1016/J.Watres.2009.09.061)
31. Shapiro K. 2014 Aggregation experiments raw data. Dryad (doi:10.5061/dryad.g0q01).
32. McKee JWA, Kavalieris L, Brasch DJ, Brown MT, Melton LD. 1992 Alginate content and composition of Macrocystis Pyrifera from New Zealand. J. Appl. Phycol. 4, 357-369. (doi:10.1007/bf02185794)
33. Chin WC, Orellana MV, Verdugo P. 1998 Spontaneous assembly of marine dissolved organic matter into polymer gels. Nature 391, 568-572. (doi:10.1038/35345)
34. Myklestad SM. 1995 Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci. Total Environ. 165, 155-164. (doi:10.1016/0048-9697(95)0 4549-g)
35. Passow U, Alldredge AL. 1994 Distribution, size and bacterial colonization of transparent exoploymer particles (TEP) in the ocean. Mar. Ecol. Progr. Ser. 113, 185-198. (doi:10.3354/meps113185)
36. Ramaiah N, Yoshikawa T, Furuya K. 2001 Temporal variations in transparent exopolymer particles (TEP) associated with a diatom spring bloom in a subarctic ria in Japan. Mar. Ecol. Progr. Ser. 212, 79-88. (doi:10.3354/meps212079)
37. Decho AW. 1990 Microbial exoploymer secretions in ocean environments-their role(s) in food webs and marine processes. Oceanogr. Mar. Biol. 28, 73-153.
38. Prinz K, Kelly TC, O'Riordan RM, Culloty SC. 2009 Non-host organisms affect transmission processes in two common trematode parasites of rocky shores. Mar. Biol. 156, 2303-2311. (doi:10.1007/s00227- 009-1258-2)
39. Marsollier L et al. 2004 Aquatic snails, passive hosts of Mycobacterium ulcerans. Appl. Environ. Microbiol. 70, 6296-6298. (doi:10.1128/aem.70.10.6296- 6298.2004)
40. Long RA, Azam F. 1996 Abundant proteincontaining particles in the sea. Aquat. Microb. Ecol. 10, 213-221. (doi:10.3354/ame010213)
41. Arkush KD et al. 2003 Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). Int. J. Parasitol. 33, 1087-1097. (doi:10.1016/S0020-7519(03) 00181-4)
42. Lindsay DS, Phelps KK, Smith SA, Flick G, Sumner SS, Dubey JP. 2001 Removal of Toxoplasma gondii oocysts from sea water by eastern oysters (Crassostrea virginica). J. Eukaryot. Microbiol. 48, 197S-198S. (doi:10.1111/j.1550-7408.2001. tb00517.x)
43. Massie GN, Ware MW, Villegas EN, Black MW. 2010 Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Vet. Parasitol. 169, 296-303. (doi:10.1016/j.vetpar. 2010.01.002)
44. Jackson J. 2008 Ecological extinction and evolution in the brave new ocean. Proc. Natl Acad. Sci. USA 105, 11 458-11 465. (doi:10.1073/pnas. 0802812105)
45. Fayer R, Dubey JP, Lindsay DS. 2004 Zoonotic protozoa: from land to sea. Trends Parasitol. 20, 531-536. (doi:10.1016/j.pt.2004.08.008)
46. Miller WA et al. 2006 Salmonella spp., Vibrio spp., Clostridium perfringens, and Plesiomonas shigelloides in marine and freshwater invertebrates from coastal California ecosystems. Microb. Ecol. 52, 198-206. (doi:10.1007/s00248-006-9080-6)
47. Cheng PKC, Wong DKK, Chung TWH, Lim WWL. 2005 Norovirus contamination found in oysters worldwide. J. Med. Virol. 76, 593-597. (doi:10. 1002/jmv.20402)
48. Ducklow HW, Mitchell R. 1979 Composition of mucus released by coral-reef coelenterates. Limnol. Oceanogr. 24, 706-714. (doi:10.4319/lo. 1979.24.4.0706)
49. Decho AW. 2000 Microbial biofilms in intertidal systems: an overview. Cont. Shelf Res. 20, 1257-1273. (doi:10.1016/s0278-4343(00)00022-4)