Investigation of viruses in Diporeia spp. from the Laurentian Great Lakes and Owasco Lake as potential stressors of declining populations

Journal of Great Lakes Research

Volumn 39, Issue 3, 2013, Pages 499-506

  Hewson, Ian ^a   Eaglesham, James B ^a   Höök, Tomas O ^b   LaBarre, Brenna A ^a   Sepúlveda, Maria S ^b   Thompson, Philip D ^a   Watkins, James M ^c   Rudstam, Lars G ^c  

^a Cornell University ^*  (United States)

^b PURDUE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

Benthic; Circovirus; Diporeia; Virus

Indexed keywords

BENTHIC; CIRCOVIRUS; DIPOREIA; FRESH WATER LAKES; LAURENTIAN GREAT LAKES; METAGENOMIC LIBRARIES; ORDERS OF MAGNITUDE; QUANTITATIVE PCR;

BACTERIOPHAGES; POLYMERASE CHAIN REACTION; POPULATION STATISTICS; VIRUSES;

LAKES;

BENTHOS; COMMUNITY COMPOSITION; DNA; ENVIRONMENTAL STRESS; EPIDEMIOLOGY; GENOME; POPULATION DECLINE; RECRUITMENT (POPULATION DYNAMICS); VIRUS;

GREAT LAKES [NORTH AMERICA]; NEW YORK [UNITED STATES]; OWASCO LAKE; UNITED STATES;

AMPHIPODA; BACTERIA (MICROORGANISMS); CIRCOVIRUS; DIPOREIA; DNA VIRUSES; DREISSENIDAE;

EID: 84883254174     PISSN: 03801330     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jglr.2013.06.006     Document Type: Article

References (70)

1. Angly F.E., Felts B., Breitbart M., Salamon P., Edwards R.A., Carlson C., Chan A., Haynes M., Kelley S., Liu H., Mahaffy J., Mueller J., Nulton J., Olson R., Parsons R., Rayhawk S., Suttle C., Rohwer F. The marine viromes of four oceanic regions. PLoS Biol. 2006, 4:2121-2131.
2. Auer N.A., Cannon B.A., Auer M.T. Life history, distribution, and production of Diporeia near the Keweenaw Peninsula Lake Superior. J. Great Lakes Res. 2009, 35:579-590.
3. Barbiero R.P., Schmude K., Lesht B.M., Riseng C.M., Warren G.J., Tuchman M.L. Trends in Diporeia populations across the Laurentian Great Lakes, 1997-2009. J. Great Lakes Res. 2011, 37:9-17.
4. Bergoin M., Mialhe E., Quiot J.M., Vanrosieren P. A Chloriridovirus (Iridoviridae) infection in populations of the planktonic crustacean Daphnia magna (Straus) (Cladocera) from salt marshes. C.R. Acad. Sci., Ser. II 1984, 298:139-142.
5. Bonami J.R., Hasson K.W., Mari J., Poulos B.T., Lightner D.V. Taura syndrome of marine penaeid shrimp: characterization of the viral agent. J. Gen. Virol. 1997, 78:313-319.
6. Bratbak G., Heldal M., Thingstad T.F., Riemann B., Haslund O.H. Incorporation of viruses into the budget of microbial C-transfer. Mar. Ecol. Prog. Ser. 1992, 83:273-280.
7. Breitbart M., Salamon P., Andresen B., Mahaffy J., Segall A., Mead D., Azam F., Rohwer F. Genomic analysis of uncultured marine viral communities. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14250-14255.
8. Breitbart M., Hewson I., Felts B., Mahaffy J.M., Nulton J., Salamon P., Rohwer F. Metagenomic analyses of an uncultured viral community from human feces. J. Bacteriol. 2003, 185:6220-6223.
9. Breitbart M., Felts B., Kelley S., Mahaffy J.M., Nulton J., Salamon P., Rohwer F. Diversity and population structure of a near-shore marine-sediment viral community. Proc. R. Soc. Lond. B 2004, 271:565-574.
10. Breitbart M., Hoare A., Nitti A., Siefert J., Haynes M., Dinsdale E., Edwards R., Souza V., Rohwer F., Hollander D. Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Cienegas, Mexico. Environ. Microbiol. 2009, 11:16-34.
11. Comps M., Mari J., Poisson F., Bonami J.R. Biophysical and biochemical properties of an unusual birnavirus pathogenic for rotifers. J. Gen. Virol. 1991, 72:1229-1236.
12. Dermott R. Sudden disappearance of the amphipod Diporeia from Eastern Lake Ontario, 1993-1995. J. Great Lakes Res. 2001, 27:423-433.
13. Dermott R., Munawar M., Bonnell R., Carou S., Niblock H., Nalepa T.F. Preliminary investigations for causes of the disappearance of Diporeia spp. from Lake Ontario. Great Lakes Fisheries Commission Technical Report 2005, 66:202-232. L.C. Mohr, T.F. Nalepa (Eds.).
14. Diemer G.S., Stedman K.M. A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol. Direct 2012, 7:13.
15. Djikeng A., Kuzmickas R., Anderson N.G., Spiro D.J. Metagenomic analysis of RNA viruses in a fresh water lake. PLoS One 2009, 4:e7264.
16. Dunlap D.S., Ng T.F.F., Rosario K., Barbosa J.G., Greco A.M., Breitbart M., et al. Molecular and microscopic evidence of viruses in marine copepods. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:1375-1380.
17. Dunn R.J.K., Welsh D.T., Jordan M.A., Teasdale P.R., Lemckert C.J. Influence of natural amphipod (Victoriopisa australiensis) (Chilton, 1923) population densities on benthic metabolism, nutrient fluxes, denitrification and DNRA in sub-tropical estuarine sediment. Hydrobiology 2009, 628:95-109.
18. Edwards R.A., Rohwer F. Viral metagenomics. Nat. Rev. Microbiol. 2005, 3:504-510.
19. Faisal M., Winters A.D. Detection of viral hemorrhagic septicemia virus (VHSV) from Diporeia spp. (Pontoporeiidae, Amphipoda) in the Laurentian Great Lakes, USA. Parasit Vectors. 2011, 4:2.
20. Fuhrman J.A. Marine viruses and their biogeochemical and ecological effects. Nature 1999, 399:541-548.
21. Gamble A.E., Hrabik T.R., Stockwell J.D., Yule D.L. Trophic connections in Lake Superior Part I: the offshore fish community. J. Great Lakes Res. 2011, 37:541-549.
22. Guiguer K.R.R.A., Barton D.R. The trophic role of Diporeia (Amphipoda) in Colpoys Bay (Georgian Bay) benthic food web: a stable isotope approach. J. Great Lakes Res. 2002, 28:228-239.
23. Hewson I., Ng G., Li W., LaBarre B.A., Aguirre I., Barbosa J.G., Breitbart M., Greco A.W., Kearns C.M., Looi A., Schaffner L.R., Thompson P.D., Hairston N.G. Metagenomic identification, seasonal dynamics and potential transmission mechanisms of a Daphnia-associated single-stranded DNA virus in two temperate lakes. Limnol. Oceanogr. 2013, (in press).
24. Hewson I., Barbosa J.G., Brown J.M., Donelan R.P., Eaglesham J.B., Eggleston E.M., LaBarre B.A. Temporal dynamics and decay of putatively allochthonous and autochthonous viral genotypes in contrasting freshwater lakes. Appl. Environ. Microbiol. 2012, 78:6583-6591.
25. Hewson I., Brown J.M., Burge C.A., Couch C.S., LaBarre B.A., Mouchka M.E., Naito M., Harvell C.D. Description of viral assemblages associated with the Gorgonia ventalina holobiont. Coral Reefs 2012, 31:487-491.
26. Kapoor A., Victoria J., Simmonds P., Slikas E., Chieochansin T., Naeem A., Shaukat S., Sharif S., Alam M.M., Angez M., Wang C.L., Shafer R.W., Zaidi S., Delwart E. A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:20482-20487.
27. Karlson K., Hulth S., Rosenberg R. Density of Monoporeia affinis and biogeochemistry in Baltic Sea sediments. J. Exp. Mar. Biol. Ecol. 2007, 344:123-135.
28. Kim K.H., Chang H.W., Nam Y.D., Roh S.W., Kim M.S., Sung Y., Jeon C.O., Oh H.M., Bae J.W. Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl. Environ. Microbiol. 2008, 74:5975-5985.
29. Kuris A.M., Poinar G.O., Hess R., Morris T.J. Virus particles in an internal parasite, Portunion conformis (Crustacea, Isopoda, Entoniscidae), and its marine crab host, Hemigrapsus oregonensis. J. Invertebr. Pathol. 1979, 34:26-31.
30. Landrum P.F., Gossiaux D.C., Nalepa T.F., Fanslow D.L. Evaluation of Lake Michigan sediment for causes of the disappearance of Diporeia spp. in southern Lake Michigan. J Great Lakes Res 2000, 26:402-407.
31. Li L.L., Kapoor A., Slikas B., Bamidele O.S., Wang C.L., Shaukat S., Masroor M.A., Wilson M.L., Ndjango J.B.N., Peeters M., Gross-Camp N.D., Muller M.N., Hahn B.H., Wolfe N.D., Triki H., Bartkus J., Zaidi S.Z., Delwart E. Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J. Virol. 2010, 84:1674-1682.
32. Madenjian C.P., Fahnenstiel G.L., Johengen T.H., Nalepa T.F., Vanderploeg H.A., Fleischer G.W., Schneeberger P.J., Benjamin D.M., Smith E.B., Bence J.R., Rutherford E.S., Lavis D.S., Robertson D.M., Jude D.J., Ebener M.P. Dynamics of the Lake Michigan food web, 1970-2000. Can. J. Fish. Aquat. Sci. 2002, 59:736-753.
33. Mari J., Bonami J.R. W2 virus infection of the crustacean Carcinus mediterraneus - a reovirus disease. J. Gen. Virol. 1988, 69:561-571.
34. Messick G.A., Overstreet R.M., Nalepa T.F., Tyler S. Prevalence of parasites in amphipods Diporeia spp. from Lakes Michigan and Huron, USA. Dis. Aquat. Org. 2004, 59:159-170.
35. Mills E.L., Casselman J.M., Dermott R., Fitzsimons J.D., Gal G., Holeck K.T., Hoyle J.A., Johannsson O.E., Lantry B.F., Makarewicz J.C., Millard E.S., Munawar I.F., Munawar M., O'Gorman R., Owens R.W., Rudstam L.G., Schaner T., Stewart T.J. Lake Ontario: food web dynamics in a changing ecosystem (1970-2000). Can. J. Fish. Aquat. Sci. 2003, 60:471-490.
36. Nalepa T.F., Fanslow D.L., Iii A.J.F., Lang G.A., Eadie B.J., Quigley M.A. Continued disappearance of the benthic amphipod Diporeia spp. in Lake Michigan: is there evidence for food limitation?. Can. J. Fish. Aquat. Sci. 2006, 63:872-890.
37. Nalepa T.F., Rockwell D.C., Schloesser D.W. Disappearance of the amphipod Diporeia spp. in the Great Lakes: workshop summary, discussion, and recommendations. NOAA Technical Reports, Ann Arbor, MI 2006, E. Glerl (Ed.).
38. Nalepa T.F., Fanslow D.L., Lang G.A. Transformation of the offshore benthic community in Lake Michigan: recent shift from the native amphipod Diporeia spp. to the invasive mussel Dreissena rostriformis bugensis. Freshwater Biol. 2009, 54:466-479.
39. Ng T.F.F., Manire C., Borrowman K., Langer T., Ehrhart L., Breitbart M. Discovery of a novel single-stranded DNA virus from a sea turtle fibropapilloma by using viral metagenomics. J. Virol. 2009, 83:2500-2509.
40. Ng T.F.F., Suedemeyer W., Wheeler E., Gulland F., Breitbart M. Novel anellovirus discovered from a mortality event of captive California sea lions. J. Gen. Virol. 2009, 90:1256-1261.
41. Ng T.F.F., Willner D., Nilsson C., Lim Y.W., Schmieder R., Chau B., Ruan Y., Rohwer F., Breitbart M. Vector-based metagenomics for animal virus surveillance. Int. J. Infect. Dis. 2010, 14:E378.
42. Ng T.F.F., Duffy S., Polston J.E., Bixby E., Vallad G.E., Breitbart M. Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLoS One 2011, 6:e19050.
43. Ng T.F.F., Willner D.L., Lim Y.W., Schmieder R., Chau B., Nilsson C., Anthony S., Ruan Y.J., Rohwer F., Breitbart M. Road surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 2011, 6:e20579.
44. Noble R.T., Fuhrman J.A. Use of SYBR Green I rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 1998, 14:113-118.
45. Proctor L.M., Fuhrman J.A. Viral mortality of marine bacteria and cyanobacteria. Nature 1990, 343:60-61.
46. Renault T., Ledeuff R.M., Cochennec N., Maffart P. Herpesviruses associated with mortalities among Pacific Oyster, Crassostrea gigas, in France - comparative study. Rev. Med. Vet-Toulouse 1994, 145:735-742.
47. Rohwer F., Edwards R. The phage proteomic tree: a genome-based taxonomy for phage. J. Bacteriol. 2002, 184:4529-4535.
48. Rosario K., Duffy S., Breitbart M. Diverse circovirus-like genome architectures revealed by environmental metagenomics. J. Gen. Virol. 2009, 90:2418-2424.
49. Rosario K., Marinov M., Stainton D., Kraberger S., Wiltshire E.J., Collings D.A., Walters M., Martin D.P., Breitbart M., Varsani A. Dragonfly cyclovirus, a novel single-stranded DNA virus discovered in dragonflies (Odonata: Anisoptera). J. Gen. Virol. 2011, 92:1302-1308.
50. Rosario K., Duffy S., Breitbart M. A field guide to eukaryotic single-stranded DNA viruses: insights gained from metagenomics. Arch. Virol. 2012, 157:1851-1871.
51. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols 2000, 365-386. Humana Press, Totowa, NJ. S. Krawertz, S. Misener (Eds.).
52. Rudstam L., Watkins J.M., Holeck K., Munawar M., Munawar I.F., Fitzpatrick M., Niblock H., Bowen K., Koops M., Lozano S., Weidel B., Walsh M., Lantry B., Stewart T., Johnson T., Schaner T., Lantry J., Connerton M., Dove A., Luckey F. Analysis of Lake Ontario Lower Aquatic food web assessment (LOLA 2003 and 2008) within the context of long-term ecological change. Report for the GLRI Funded Project Improving Lake Ontario Environmental Management Decisions (Grant ID # 97220700-0) 2012, 44.
53. Schloss P.D., Westcott S.L., Ryabin T., Hall J.R., Hartmann M., Hollister E.B., Lesniewski R.A., Oakley B.B., Parks D.H., Robinson C.J., Sahl J.W., Stres B., Thallinger G.G., Van Horn D.J., Weber C.F. Introducing mothur: open-Source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 2009, 75:7537-7541.
54. SOLEC State of the Lakes Ecosystem Conference: state of the Great Lakes 2010. State of the Great Lakes 2010, E. Canada, Agency UEP (Eds.).
55. Sprague V., Beckett R.L. A disease of blue crabs (Callinectes sapidus) in Maryland and Virginia. J. Invertebr. Pathol. 1966, 8:287-289.
56. Steward G.F., Preston C.M. Analysis of a viral metagenomic library from 200m depth in Monterey Bay, California constructed by direct shotgun cloning. Virol. J. 2011, 8:287.
57. Suttle C.A. Marine viruses - major players in the global ecosystem. Nat. Rev. Microbiol. 2007, 5:801-812.
58. Thingstad T.F., Lignell R. A theoretical approach to the question of how trophic interactions control carbon demand, growth rate, abundance and diversity. Aquat. Microb. Ecol. 1997, 13:19-27.
59. Thurber R.L.V., Correa A.M.S. Viruses of reef-building scleractinian corals. J. Exp. Mar. Biol. Ecol. 2011, 408:102-113.
60. Thurber R.L.V., Barott K.L., Hall D., Liu H., Rodriguez-Mueller B., Desnues C., Edwards R.A., Haynes M., Angly F.E., Wegley L., Rohwer F.L. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:18413-18418.
61. Thurber R.V., Haynes M., Breitbart M., Wegley L., Rohwer F. Laboratory procedures to generate viral metagenomes. Nat. Protoc. 2009, 4:470-483.
62. Vanderploeg H.A., Liebig J.R., Nalepa T.F., Fahnenstiel G.L., Pothoven S.A. Dreissena and the disappearance of the spring phytoplankton bloom in Lake Michigan. J. Great Lakes Res. 2010, 36:50-59.
63. Vogt G. Cytopathology of Bay of Piran shrimp virus (BPSV), a new crustacean virus from the Mediterranean Sea. J. Invertebr. Pathol. 1996, 68:239-245.
64. Watkins J.M., Dermott R., Lozano S.J., Mills E.L., Rudstam L.G., Scharold J.V. Evidence for remote effects of dreissenid mussels on the amphipod Diporeia: analysis of Lake Ontario Benthic Surveys, 1972-2003. J. Great Lakes Res 2007, 33:642-657.
65. Watkins J.M., Rudstam L.G., Mills E.L., Teece M.A. Coexistence of the native benthic amphipod Diporeia spp. and exotic dreissenid mussels in the New York Finger Lakes. J. Great Lakes Res. 2012, 38:226-235.
66. Weinbauer M.G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 2004, 28:127-181.
67. Widada J.S., Bonami J.R. Characteristics of the monocistronic genome of extra small virus, a virus-like particle associated with Macrobrachium rosenbergii nodavirus: possible candidate for a new species of satellite virus. J. Gen. Virol. 2004, 85:643-646.
68. Willner D., Thurber R.V., Rohwer F. Metagenomic signatures of 86 microbial and viral metagenomes. Environ. Microbiol. 2009, 11:1752-1766.
69. Wilson W.H., Tarran G.A., Schroeder D., Cox M., Oke J., Malin G. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. UK 2002, 82:369-377.
70. Wommack K.E., Bhavsar J., Polson S.W., Chen J., Dumas M., Srinivasiah S., et al. VIROME: a standard operating procedure for analysis of viral metagenome sequences. Stand. Genomic Sci. 2012, 6:421-433.