Description of viridilobus marinus (gen. et sp. nov.), a new raphidophyte from delaware's inland bays

Journal of Phycology

Volumn 48, Issue 5, 2012, Pages 1220-1231

  Demir Hilton, Elif ^a,c   Hutchins, David A ^a,d   Czymmek, Kirk J ^b   Coyne, Kathryn J ^a  

^a UNIVERSITY OF DELAWARE   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c MONTEREY BAY AQUARIUM RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Chattonella; Chattonellaceae; Delaware Inland Bays; Heterosigma; Raphidophyceae; Viridilobus

Indexed keywords

CHATTONELLA; HETEROSIGMA; HETEROSIGMA AKASHIWO; RAPHIDOPHYCEAE;

EID: 84867228447     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2012.01212.x     Document Type: Article

References (72)

1. Andersen R. A. 2004. Biology and systematics of heterokont and haptophyte algae. Am. J. Bot. 91:1508-22.
2. Black E. A., Whyte J. N. C., Bagshaw J. W. & Ginther N. G. 1991. The effects of Heterosigma akashiwo on juvenile Oncorhynchus tshawytscha and its implications for fish culture. J. Appl. Ichthyol. 7:168-75.
3. Bourdelais A. J., Tomas C. R., Naar J., Kubanek J. & Baden D. G. 2002. New fish-killing alga in coastal Delaware produces neurotoxins. Environ. Health Persp. 110:465-70.
4. Bourett, T. M., Czymmek, K. J. & Howard, R. J. 1999. Ultrastructure of chloroplast protuberances in rice leaves preserved by high-pressure freezing. Planta 208:472-9.
5. Bowers H. A., Tomas C., Tengs T., Kempton J. W., Lewitus A. J. & Oldach D. W. 2006. Raphidophyceae [Chadefaud ex Silva] systematics and rapid identification: sequence analyses and real-time PCR assays. J. Phycol. 42:1333-48.
6. Cattolico R. A. 1978. Variation on plastid number. Plant Physiol. 62:558-62.
7. Cattolico R. A., Boothroyd J. C. & Gibbs S. P. 1976. Synchronous growth and plastid replication in naturally wall-less alga Olisthodiscus luteus. Plant Physiol. 57:497-503.
8. Connell L. B. 2000. Nuclear ITS region of the alga Heterosigma akashiwo (Chromophyta: Raphidophyceae) is identical in isolates from Atlantic and Pacific basins. Mar. Biol. 136:953-60.
9. Connell L. & Cattolico R. A. 1996. Fragile algae: axenic culture of field collected samples of Heterosigma carterae. Mar. Biol. 125:421-6.
10. Coyne K. J., Handy S. M., Demir E., Whereat E. B., Hutchins D. A., Portune K. J., Doblin M. A. & Cary S. C. 2005. Improved quantitative real-time PCR assays for enumeration of harmful algal species in field samples using an exogenous DNA reference standard. Limnol. Oceanogr. Methods 3:381-91.
11. Coyne K. J., Hutchins D. A., Hare C. E. & Cary S. C. 2001. Assessing temporal and spatial variability in Pfiesteria piscicida distributions using molecular probing techniques. Aquat. Microb. Ecol. 24:275-85.
12. Cronberg G., Lindmark G. & Bjork S. 1988. Mass development of the flagellate Gonyostomum semen (Raphidophyta) in Swedish forest lakes, an effect of acidification. Hydrobiologia 161:217-36.
13. Demir E., Coyne K., Doblin M., Handy S. & Hutchins D. 2008. Assessment of microzooplankton grazing on Heterosigma akashiwo using a species- specific approach combining quantitative real-time PCR (QPCR) and dilution methods. Microb. Ecol. 55:583-94.
14. Dempster E. L., Pryor K. V., Francis D., Young J. E. & Rogers H. J. 1999. Rapid DNA extraction from ferns for PCR-based analyses. Biotechniques 27:66-8.
15. Demura M., Noël M.-H., Kasai F., Watanabe M. M. & Kawachi M. 2009. Taxonomic revision of Chattonella antiqua, C. marina and C. ovata (Raphidophyceae) based on their morphological characteristics and genetic diversity. Phycologia 48:518-35.
16. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F. et al. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 1:36. (Web Server issue):W465-9.
17. Dorantes-Aranda J. J., Waite T. D., Godrant A., Rose A. L., Tovar C. D., Woods G. M. & Hallegraeff G. M. 2011. Novel application of a fish gill cell line assay to assess ichthyotoxicity of harmful marine microalgae. Harmful Algae 10:366-73.
18. Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17:368-76.
19. Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-91.
20. Fredrickson K. A., Strom S. L., Crim R. & Coyne K. J. 2011. Interstrain variability in physiology and genetics of Heterosigma akashiwo (Raphidophyceae) from the West Coast of North America. J. Phycol. 47:25-35.
21. Guillard, R. 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. L. & Chanley, M. H. [Ed.] Culture of Marine Invertebrate Animals. Plenum Press, New York, pp. 26-60.
22. Hada Y. 1967. Protozoan plankton of the Inland Sea, Setonaikai. I. The Mastigophora. Bull. Suzugamine Woman's Coll. Nat. Sci. 13:1-26.
23. Hada Y. 1968. Protozoan plankton of the Inland Sea, Setonaikai. II. The Mastigophora and Sarcodina. Bull. Suzugamine Woman's Coll. Nat. Sci. 14:1-28.
24. Handy S. M., Coyne K. J., Portune K. J., Demir E., Doblin M. A., Hare C. E., Cary S. C. & Hutchins D. A. 2005. Evaluating vertical migration behavior of harmful raphidophytes in the Delaware Inland Bays utilizing quantitative real-time PCR. Aquat. Microb. Ecol. 40:121-32.
25. Handy, S. M., Hutchins, D. A., Cary, S. C. & Coyne, K. J. 2006. Simultaneous enumeration of multiple raphidophyte species by quantitative real-time PCR: capabilities and limitations. Limnol. Oceanogr. Meth. 4:193-204.
26. Haque S. M. & Onoue Y. 2002. Variation in toxin compositions of two harmful raphidophytes, Chattonella antiqua and Chattonella marina, at different salinities. Environ. Toxicol. 17:113-8.
27. Hara Y. & Chihara M. 1987. Morphology, ultrastructure and taxonomy of the Raphidophycean alga Heterosigma akashiwo. Bot. Mag. Tokyo 100:151-63.
28. Hara Y., Doi K. & Chihara M. 1994. Four new species of Chattonella (Raphidophyceae, Chromophyta) from Japan. Jpn. J. Phycol. 42:407-20.
29. Hara Y., Inouye I. & Chihara M. 1985. Morphology and ultrastructure of Olisthodiscus luteus (Raphidophyceae) with special reference to the taxonomy. Bot. Mag. Tokyo 98:251-62.
30. Hashimoto H. 1997. Electron-opaque annular structure girdling the constricting isthmus of the dividing chloroplasts of Heterosigma akashiwo (Raphidophyceae, Chromophyta). Protoplasma 197:210-6.
31. Van Heukelem L. & Thomas C. S. 2001. Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments. J. Chromatogr. A 910:31-49.
32. Heywood, P. 1990. Phylum Raphidophyta. In Margulis, L., Corliss, J. O., Melkonian, M. & Chapman, D. J. [Eds.] Handbook of Protoctista. Jones & Bartlett, Boston, Massachusetts, pp. 318-25.
33. Hiroishi S., Okada H., Imai I. & Yoshida T. 2005. High toxicity of the novel bloom-forming species Chattonella ovata (Raphidophyceae) to cultured fish. Harmful Algae 4:783-7.
34. Horiguchi T. 1996. Haramonas dimorpha gen. et sp. nov. (Raphidophyceae), a new marine raphidophyte from Australian mangrove. Phycol. Res. 44:143-50.
35. Horner R. A., Garrison D. L. & Plumley F. G. 1997. Harmful algal blooms and red tide problems on the US west coast. Limnol. Oceanogr. 42:1076-88.
36. Hosoi-Tanabe S., Honda D., Fukaya S., Otake I., Inagaki Y. & Sako Y. 2007. Proposal of Pseudochattonella verruculosa gen. nov., comb. nov. (Dictyochophyceae) for a former raphidophycean alga Chattonella verruculosa, based on 18S rDNA phylogeny and ultrastructural characteristics. Phycol. Res. 55:185-92.
37. Hulburt E. M. 1965. Flagellates from brackish waters in the vicinity of Woods Hole. Massachusetts. J. Phycol. 1:87-94.
38. Imai I. & Itoh K. 1987. Annual life-cycle of Chattonella spp., causative flagellates of noxious red tides in the Inland Sea of Japan. Mar. Biol. 94:287-92.
39. Ishida H., Nozawa A., Nukaya H. & Tsuji K. 2004. Comparative concentrations of brevetoxins PbTx-2, PbTx-3, BTX-B1 and BTX-B5 in cockle, Austrovenus stutchburyi, greenshell mussel, Perna canaliculus, and Pacific oyster, Crassostrea gigas, involved neurotoxic shellfish poisoning in New Zealand. Toxicon 43:779-89.
40. Keppler C. J., Lewitus A. J., Ringwood A. H., Hoguet J. & Staton T. 2006. Sublethal cellular effects of short-term raphidophyte and brevetoxin exposures on the eastern oyster Crassostrea virginica. Mar. Ecol. Prog. Ser. 312:141-7.
41. Khan S., Arakawa O. & Onoue Y. 1996. Neurotoxin production by a chloromonad Fibrocapsa japonica (Raphidophyceae). J. World Aquacult. Soc. 27:254-63.
42. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F. et al. 2007. ClustalW and ClustalX version 2. Bioinformatics 3:2947-8.
43. Lewitus A. J., Schmidt L. B., Mason L. J., Kempton J. W., Wilde S. B., Wolny J. L., Williams B. J., Hayes K. C., Hymel S. N., Keppler C. J. & Ringwood A. H. 2003. Harmful algal blooms in South Carolina residential and golf course ponds. Popul. Environ. 24:387-413.
44. Ling C. & Trick C. G. 2010. Expression and standardized measurement of hemolytic activity in Heterosigma akashiwo. Harmful Algae 9:522-9.
45. Marshall J. A., Nichols P. D., Hamilton B., Lewis R. J. & Hallegraeff G. M. 2003. Ichthyotoxicity of Chattonella marina (Raphidophyceae) to damselfish (Acanthochromis polycanthus): the synergistic role of reactive oxygen species and free fatty acids. Harmful Algae 2:273-81.
46. Marshall J. A., Ross T., Pyecroft S. & Hallegraeff G. 2005b. Superoxide production by marine microalgae - II. Towards understanding ecological consequences and possible functions. Mar. Biol. 147:541-9.
47. Marshall J. A., de Salas M., Oda T. & Hallegraeff G. 2005a. Superoxide production by marine microalgae. Mar. Biol. 147:533-40.
48. Medlin L., Elwood H. J., Stickel S. & Sogin M. L. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491-9.
49. Mostaert A. S., Karsten U., Hara Y. & Watanabe M. M. 1998. Pigments and fatty acids of marine raphidophytes: a chemotaxonomic re-evaluation. Phycol. Res. 46:213-20.
50. Nylander, J. A. A. 2004. MrAIC.pl. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
51. Plakas S. M., Wang Z. H., El Said K. R., Jester E. L. E., Granade H. R., Flewelling L., Scott P. & Dickey R. W. 2004. Brevetoxin metabolism and elimination in the Eastern oyster (Crassostrea virginica) after controlled exposures to Karenia brevis. Toxicon 44:677-85.
52. Portune, K. J., Coyne, K. J., Hutchins, D. A., Handy, S. M. & Cary, S. C. 2009. Quantitative real-time PCR for detecting germination of Heterosigma akashiwo and Chattonella subsalsa cysts from Delaware's Inland Bays, USA. Aquat. Microb. Ecol. 55:229-39.
53. Potter D., Saunders G. W. & Andersen R. A. 1997. Phylogenetic relationships of the Raphidophyceae and Xanthophyceae as inferred from nucleotide sequences of the 18S ribosomal RNA gene. Am. J. Bot. 84:966-72.
54. Rensel J. E. J., Haigh N. & Tynan T. J. 2010. Fraser river sockeye salmon marine survival decline and harmful blooms of Heterosigma akashiwo. Harmful Algae 10:98-115.
55. Saitou N. & Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-25.
56. Smayda, T. 1998. Ecophysiology and bloom dynamics of Heterosigma akashiwo (Raphidophyceae). In Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. [Eds.] Physiological Ecology of Harmful Algal Blooms. Sringer-Verlag, Berlin, pp. 113-31.
57. Stevenson R. J. 1984. Procedures for mounting algae in a syrup medium. Trans. Am. Microsc. Soc. 103:320-1.
58. Tamura K., Dudley J., Nei M. & Kumar S. 2007. MEGA4: molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-9.
59. Tamura K. & Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10:512-26.
60. Tamura K., Nei M. & Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101:11030-5.
61. Taylor, E. J. R. 1990. Red tides, brown tides and other harmful algal blooms: the view into the 1990s. In Granéli, E., Sundström, B., Edler, L. & Anderson, D. M. [Eds.] Toxic Marine Phytoplankton. Elsevier, New York, pp. 527-33.
62. Thompson J. D., Higgins D. G. & Gibson T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-80.
63. Throndsen J. 1996. Note on the taxonomy of Heterosigma akashiwo (Raphidophyceae). Phycologia 35:367.
64. Twiner M. J., Dixon S. J. & Trick C. G. 2004. Extracellular organics from specific cultures of Heterosigma akashiwo (Raphidophyceae) irreversibly alter respiratory activity in mammalian cells. Harmful Algae 3:173-82.
65. Twiner M. J. & Trick C. G. 2000. Possible physiological mechanisms for production of hydrogen peroxide by the ichthyotoxic flagellate Heterosigma akashiwo. J. Plankton Res. 22:1961-75.
66. Tyrrell, J. V., Bergquist, P. R., Bergquist, P. L. & Scholin, C. A. 2001. Detection and enumeration of Heterosigma akashiwo and Fibrocapsa japonica (Raphidophyceae) using rRNA-targeted oligonucleotide probes. Phycologia 40:457-67.
67. Vesk M. & Moestrup O. 1987. The flagellar root-system in Heterosigma akashiwo (Raphidophyceae). Protoplasma 137:15-28.
68. Whereat, E. 2005. Phytoplankton Monitoring Report. Volunteer Phytoplankton Monitoring Group, Delaware Inland Bays Citizen Monitor Program. University of Delaware, Sea Grant Marine Advisory Service, Lewes, Delaware.
69. Yamaguchi H., Hoppenrath M., Takishita K. & Horiguchi T. 2008. Haramonas pauciplastida sp. nov. (Raphidophyceae, Heterokontophyta) and phylogenetic analyses of Haramonas species using small subunit ribosomal RNA gene sequences. Phycol. Res. 56:127-38.
70. Yamaguchi H., Nakayama T., Murakami A. & Inouye I. 2010. Phylogeny and taxonomy of the Raphidophyceae (Heterokontophyta) and Chlorinimonas sublosa gen. et sp. nov., a new marine sand-dwelling raphidophyte. J. Plant. Res. 123:333-42.
71. Yang C. Z., Albright L. J. & Yousif A. N. 1995. Oxygen radical mediated effects of the toxic phytoplankter Heterosigma carterae on juvenile rainbow trout Oncorhynchus mykiss. Dis. Aquat. Org. 23:101-8.
72. Zhang Y., Fu F. X., Whereat E., Coyne K. J. & Hutchins D. A. 2006. Bottom-up controls on a mixed-species HAB assemblage: a comparison of sympatric Chattonella subsalsa and Heterosigma akashiwo (Raphidophyceae) from the Delaware Inland Bays, USA. Harmful Algae 5:310-20.