Ecological aspects of viral infection and lysis in the harmful brown tide alga Aureococcus anophagefferens

Aquatic Microbial Ecology

Volumn 47, Issue 1, 2007, Pages 25-36

  Gobler, Christopher J ^a   Anderson, O Roger ^b   Gastrich, Mary Downes ^b   Wilhelm, Steven W ^c  

^a STONY BROOK UNIVERSITY   (United States)

^b Department of Earth and Environmental Sciences   (United States)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Algal viruses; Aureococcus anophagefferens; Brown tide; Harmful algal blooms; Strain specificity; Viral infection; Viral resistance

Indexed keywords

ALGAE; AUREOCOCCUS ANOPHAGEFFERENS;

EID: 34548299907     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame047025     Document Type: Article

References (64)

1. Anderson DM, Glibert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704-726
2. Bailey CJ, Andersen RA (1999) Analysis of clonal cultures of the brown tide algae Aureococcus and Aureoumbra (Pelagophyceae) using 18S rRNA, rbcL and RUBISCO spacer sequences. J Phycol 35:570-574
3. Baudoux AC, Brussaard CPD (2005) Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa. Virology 341:80-90
4. Berg GM, Repeta DJ, LaRoche J (2002) Dissolved organic nitrogen hydrolysis rates in axenic cultures of Aureococcus anophagefferens (Pelagophyceae): comparison with heterotrophic bacteria. Appl Environ Microbiol 68:401-404
5. Bettarel Y, Kan J, Wang K, Williamson KE and 5 others (2005) Isolation and preliminary characterisation of a small nuclear inclusion virus infecting the diatom Chaetoceros cf. gracilis. Aquatic Microb Ecol 40:103-114
6. Brussaard CPD (2004) Viral control of phytoplankton populations - a review. J Eukaryotic Microbiol 51:125-138
7. Caron DA, Dennett MR, Moran DM, Schaffner RA, Lonsdale DJ, Gobler CJ, Nuzzi R, McLean TI (2003) Development and application of a monoclonal-antibody technique for counting Aureococcus anophagefferens, an alga causing recurrent brown tides in the Mid-Atlantic United States. Appl Environ Microbiol 69:5492-5502
8. Cerrato RM, Caron DA, Lonsdale DJ, Rose JM, Schaffner RA (2004) An experimental approach to examine the effect of the hard clam Mercenaria mercenaria on the development of blooms of the brown tide alga Aureococcus anophagefferens. Mar Ecol Prog Ser 281:93-108
9. Colin SP, Dam HG (2002) Latitudinal differentiation in the effects of the toxic dinoflagellate Alexandrium spp. on the feeding and reproduction of populations of the copepod Acartia hudsonica. Harmful Algae 1:113-125
10. Cosper EM, Dennison WC, Carpenter EJ, Bricelj VM, Mitchell JG, Kuenstner SH, Colflesh DC, Dewey M (1987) Recurrent and persistent 'brown tide' blooms perturb coastal marine ecosystem. Estuaries 10:284-290
11. Cosper EM, Dennison WC, Milligan AJ, Carpenter EJ, Lee C, Holzapfel J, Milanese L (1989) An examination of the environmental factors important to initiating and sustaining -brown tide- blooms. In: Cosper EM, Bricelj VM, Carpenter EJ (eds) Novel phytoplankton blooms: causes and impacts of recurrent brown tides and other unusual blooms. Springer, New York, p 317-340
12. Cosper EM, Garry RT, Milligan AJ, Doall MH (1993) Iron, selenium and citric acid are critical to the growth of the 'brown tide' microalga Aureococcus anophagefferens. In: Toxic phytoplankton blooms in the sea. Proc 5th Int Conf Toxic Marine Phytoplankton. Elsevier, Amsterdam, p 667-673
13. Cottrell MT, Suttle CA (1991) Wide-spread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan eucaryotic marine phytoplankter, Micromonas pusilla. Mar Ecol Prog Ser 78:1-9
14. DeYoe HR, Chan AM, Suttle CA (1995) Phylogeny of Aureococcus anophagefferens and a morphologically similar bloom-forming alga from Texas as determined by 18S ribosomal RNA sequence analysis. J Phycol 31:413-418
15. Garry RT, Hearing P, Cosper EM (1998) The characterization of a lytic virus infectious to the brown tide microalga, Aureococcus anophagefferens (Chrysophyceae). J Phycol 34:616-621
16. Gastrich MD, Anderson OR, Benmayor SS, Cosper EM (1998) Ultrastructural analysis of viral infection in the brown-tide alga, Aureococcus anophagefferens (Pelagophyceae). Phycologia 37:300-306
17. Gastrich MD, Anderson OR, Cosper EM (2002) Viral-like particles (VLPS) in the alga, Aureococcus anophagefferens (Pelagophyceae), during 1999-2000 brown tide blooms in Little Egg Harbor, New Jersey. Estuaries 25:938-943
18. Gastrich, MD, Bell JL, Gobler CJ, Anderson OR, Wilhelm SW (2004) Viruses as potential regulators of regional brown tide blooms caused by the alga, Aureococcus anophagefferens: a comparison of bloom years 1999-2000 and 2002. Estuaries 27:112-119
19. Gobler CJ, Sañudo-Wilhelmy SA (2001) Temporal variability of groundwater seepage and brown tide blooms in a Long Island embayment. Mar Ecol Prog Ser 217:299-309
20. Gobler CJ, Sañudo-Wilhelmy SA (2003) Cycling of colloidal organic carbon and nitrogen during estuarine plankton blooms. Limnol Oceanogr 48:2314-2320
21. Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sañudo-Wilhelmy SA (1997) Cycling and bioavailability of C, N, P, Fe and Se released by viral lysis of a marine chrysophyte. Limnol Oceanogr 42:1492-1504
22. Gobler CJ, Renaghan MJ, Buck NJ (2002) Impacts of nutrients and grazing mortality on the abundance of Aureococcus anophagefferens during a New York brown tide bloom. Limnol Oceanogr 47:129-141
23. Gobler CJ, Deonarine SN, Leigh-Bell J, Gastrich MD, Anderson OR, Wilhelm SW (2004) Ecology of phytoplankton communities dominated by Aureococcus anophagefferens: The role of viruses, nutrients, and microzooplankton grazing. Harmful Algae 3:471-483
24. Gobler CJ, Lonsdale DJ, Boyer GL (2005) A synthesis and review of causes and impact of harmful brown tide blooms caused by the alga, Aureococcus anophagefferens. Estuaries 28:726-749
25. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229-239
26. Juneau P, Lawrence JE, Suttle CA, Harrison PJ (2003) Effects of viral infection on photosynthetic processes in the bloom-forming alga Heterosigma akashiwo. Aquat Microb Ecol 31: 9-17
27. Kobler ZS, Zehr J, Falkowski PG (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Limnol Oceanogr 38:1646-1665
28. Lawrence JE, Chan AM, Suttle CA (2001) A novel virus (HaNIV) causes lysis of the toxic bloom-forming alga Heterosigma akashiwo (Raphidophyceae). J Phycol 37:216-222
29. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86-89
30. Lomas MW, Glibert PM, Berg GM, Burford M (1996) Characterization of nitrogen uptake by natural populations of Aureococcus anophagefferens (Chrysophyceae) as a function of incubation duration, substrate concentration, light, and temperature. J Phycol 32:907-916
31. MacKenzie JJ, Haselkorn R (1972) Photosynthesis and the development of blue green algal virus SM-1. Virology 49:517-521
32. Milligan AJ, Cosper EM (1997) Growth and photosynthesis of the 'brown tide' microalga Aureococcus anophagefferens in subsaturating constant and fluctuating irradiance. Mar Ecol Prog Ser 153:67-75
33. Milligan KLD, Cosper EM (1994) Isolation of virus capable of lysing the brown tide microalga, Aureococcus anophagefferens. Science 266:805-807
34. Mulholland MR, Gobler CJ, Lee C (2002) Peptide hydrolysis, amino acid oxidation and N uptake in communities seasonally dominated by Aureococcus anophagefferens. Limnol Oceanogr 47:1094-1108
35. Murray AG, Jackson GA (1992) Viral dynamics - a model of the effects of size, shape, motion, and abundance of single-celled planktonic organisms and other particles. Mar Ecol Prog Ser 89:103-116
36. Nagasaki K, Yamaguchi M (1997) Isolation of a virus infectious to the harmful bloom causing microalga Heterosigma akashiwo (Raphidophyceae). Aquat Microb Ecol 13:135-140
37. Nagasaki K, Yamaguchi M (1998) Intra-species host specificity of HaV (Heterosigma akashiwo virus) clones. Aquat Microbiol Ecol 14:109-112
38. Nagasaki K, Ando M, Imai I, Itakura S, Ishida Y (1994) Virus-like particles in Heterosigma akashiwo (Raphidophyceae): a possible red tide disintegration mechanism. Mar Biol 119:307-312
39. Nagasaki K, Tomaru Y, Tarutani K, Katanozaka N, Yamanaka S, Tanabe H, Yamaguchi M (2003) Growth characteristics and intraspecies host specificity of a large virus infecting the dinoflagellate Heterocapsa circulatisquama. Appl Environ Microbiol 69:2580-2586
40. Noble RT, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14:113-118
41. Parkhill JP, Maillet G, Cullen JJ (2001) Fluorescence based maximal quantum yield for photosystem II as a diagnostic of nutrient limitation. J Phycol 37:517-529
42. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford
43. Pitcher GC, Calder D (2000) Harmful algal blooms of the southern Benguela Current: a review and appraisal of monitoring from 1989 to 1997. S Afr J Mar Sci 22:255-271
44. Porter KG, Feig YS (1980). The use of DAPI for identifying and counting microflora. Limnol Oceanogr 25: 943-948
45. Rabinovitch A, Aviram I, Zaritsky A (2003) Bacterial debris - an ecological mechanism for coexistence of bacteria and their viruses. J Theor Biol 224: 377-383
46. Schroeder DC, Oke J, Malin G, Wilson WH (2002) Coccolithovirus (Phycodnaviridae): characterization of a new large dsDNA algal virus that infects Emiliania huxleyi. Arch Virol 147:1685-1698
47. Sengco MR, Anderson DM (2004) Controlling harmful algal blooms through clay flocculation. J Eukaryot Microbiol 51:169-172
48. Sherman LA (1976) Infection of Synechococcus cedrorum by the cyanophage AS-1M. Virology 71:199-206
49. Sieburth JMN, Johnson PW, Hargraves PE (1988) Ultrastructure and ecology of Aureococcus anophagefferens gen. et sp. nov. (Chrysophyceae): the dominant picoplankter during a bloom in Narragansett Bay, Rhode Island. Summer 1985. J Phycol 24:416-425
50. Smayda TJ (1990) Novel and nuisance phytoplankton blooms in the sea: Evidence for a global epidemic. In: Granéli E, Sundstrom B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier, New York, p 29-40
51. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. WH Freeman & Co, New York
52. Sullivan MB, Waterbury JB, Chisholm SW (2003) Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047-1051
53. Sunda WG, Granéli E, Gobler CJ (2006) Positive feedback and the development and persistence of ecosystem disruptive algal blooms. J Phycol 42:963-974
54. Suttle CA (2005) Viruses in the sea. Nature 437:356-361
55. Suttle CA, Chan AM (1993) Marine cyanophages infecting oceanic and coastal strains of Synechococcus - abundance, morphology, cross- infectivity and growth characteristics. Mar Ecol Prog Ser 92: 99-109
56. Suttle CA, Chan AM (1995) Viruses infecting the marine prymnesiophyte Chrysochromulina spp.: isolation, preliminary characterization and natural abundance. Mar Ecol Prog Ser 118:275-282
57. Tarutani K, Nagasaki K, Yamaguchi M (2000) Viral impacts on total abundance and clonal composition of harmful bloom-forming phytoplankton Heterosigma akashiwo. Appl Environ Microbiol 66:4916-4920
58. Tarutani K, Nagasaki K, Itakura S, Yamaguchi M (2001) Isolation of a virus infecting the novel shellfish-killing dinoflagellate Heterocapsa circularisquama. Aquat Microb Ecol 23:101-111
59. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13:19-27
60. Thyrhaug R, Larsen A, Thingstad TF, Bratbak G (2003) Stable coexistence in marine algal host-virus systems. Mar Ecol Prog Ser 254:27-35
61. Wilhelm SW, Poorvin L (2001) Quantification of algal viruses in marine samples. In: Paul JH (ed) Methods in microbiology, Vol 30. Marine microbiology. Academic Press, New York, p 53-66
62. Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea. BioScience 49:781-788
63. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Molecular Biol Rev 64:69-114
64. Zingone A, Natale F, Biffali E, Borra M, Forlani G, Sarno D (2006) Diversity in morphology, infectivity, molecular characteristics and induced host resistance between two viruses infecting Micromonas pusilla. Aquat Microb Ecol 45:1-14