Molecular phylogenetic analysis of the heterotrophic chrysophyte genus Paraphysomonas (Chrysophyceae), and the design of rRNA-targeted oligonucleotide probes for two species

Journal of Phycology

Volumn 35, Issue 4, 1999, Pages 824-837

  Caron, David A ^a   Lim, Ee Lin ^a   Dennett, Mark R ^a   Gast, Rebecca J ^a   Kosman, Carol ^b   DeLong, Edward F ^c  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MONTEREY BAY AQUARIUM RESEARCH INSTITUTE   (United States)

Author keywords

18S rRNA; Chrysophyte; In situ hybridization; Microbial ecology; Nanoflagellate; Oligonucleotide probe; Paraphysomonas; Protistan biogeography; Protistan phylogeny; Protozoa

Indexed keywords

ALGA GENETICS; IDENTIFICATION; MOLECULAR GENETICS; OLIGONUCLEOTIDE PROBE; PHYLOGENETIC ANALYSIS; RIBOSOMAL RNA;

ALGAE; CHRYSOPHYCEAE; EUKARYOTA; FORAMINIFERA; PARAPHYSOMONAS; PARAPHYSOMONAS BANDAIENSIS; PARAPHYSOMONAS FORAMINIFERA; PARAPHYSOMONAS IMPERFORATA; PARAPHYSOMONAS VESTITA; PROKARYOTA; PROTISTA; PROTOZOA;

EID: 0345411432     PISSN: 00223646     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1529-8817.1999.3540824.x     Document Type: Article

References (77)

1. Andersen, O. K., Goldman, J. C., Caron, D. A. & Dennett, M. R. 1986. Nutrient cycling in a microflagellate food chain: III. Phosphorus dynamics. Mar. Ecol. Prog. Ser. 31:47-55.
2. Andersen, P. & Sørensen, H. M. 1986. Population dynamics and trophic coupling in pelagic microorganisms in eutrophic coastal systems. Mar. Ecol. Prog. Ser. 33:99-109.
3. Andersen, R. A., Saunders, G. W., Paskind, M. P. & Sexton, J. P. 1993. Ultrastructure and 18S rRNA gene sequence for Pelagomonas calceolata gen. et sp. nov. and the description of a new algal class, the Pelagophyceae classis nov. J. Phycol. 29: 701-15.
4. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A. & Thingstad, F. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10:257-63.
5. Bhattacharya, D., Medlin, L., Wainright, P. O., Ariztia, E. V., Bibeau, C., Stickel, S. K. & Sogin, M. L. 1992. Algae containing chlorophylls a + c are paraphyletic: molecular evolutionary analysis of the Chromophyta. Evolution 46:1801-17.
6. Booth, B. C., Lewin, J. & Norris, R. E. 1982. Nanoplankton species predominant in the subarctic Pacific in May and June 1978. Deep-Sea Res. 29:185-200.
7. Burkholder, J. M. & Glasgow, H. B., Jr. 1997. Trophic controls on stage transformations of a toxic ambush-predator dinoflagellate. J. Eukaryot. Microbiol. 44:200-5.
8. Caron, D. A. 1993. Enrichment, isolation, and culture of free-living heterotrophic flagellates. In Kemp, P. F. Sherr, B. F., Sherr, E. B. & Cole, J. J. [Eds.] Handbook of Methods In Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, pp. 77-89.
9. _ 1997. Protistan community structure. In Hurst, C. J., Knudsen, G. R., McInerney, M. J., Stetzenbach, L. D. & Walter, M. V. [Eds.] Manual of Environmental Microbiology. ASM Press, Washington, D.C., pp. 284-94.
10. Caron, D. A. & Finlay, B. J. 1994. Protozoan links in food webs. In Hausmann, K. & Hülsmann, N. [Eds.] Progress in Protozoology, Proceedings of the IX International Congress of Protozoology, Berlin 1993. Gustav Fischer Verlag, Stuttgart, pp. 125-30.
11. Caron, D. A., Goldman, J. C., Andersen, O. K. & Dennett, M. R. 1985. Nutrient cycling in a microflagellate food chain. II. Population dynamics and carbon cycling. Mar. Ecol. Prog. Ser. 24:243-54.
12. Caron, D. A., Goldman, J. C. & Dennett, M. R. 1986. Effect of temperature on growth, respiration, and nutrient regeneration by an omnivorous microflagellate. Appl. Environ. Microbiol. 52:1340-7.
13. _ 1990. Carbon utilization by the omnivorous flagellate Paraphysomonas imperforata. Limnol. Oceanogr. 35:192-201.
14. Cedhagen, T. & Tendal, O. S. 1989. Evidence of test detachment in Astrorhiza limicola, and two consequential synonyms: Amoeba gigantea and Megamoebomyxa argillobia (Foraminiferida). Sarsia 74:195-200.
15. Davis, P. G., Caron, D. A., Johnson, P. W. & Sieburth, J. M. 1985. Phototrophic and apochlorotic components of picoplankton and nanoplankton in the North Atlantic: geographic, vertical, seasonal and diel distributions. Mar. Ecol. Prog. Ser. 21:15-26.
16. Davis, P. G. & Sieburth, J. M. 1984. Estuarine and oceanic microflagellate predation of actively growing bacteria: estimation by frequency of dividing-divided bacteria. Mar. Ecol. Prog. Ser. 19:237-46.
17. DeLong, E. F. 1991. Molecular Systematics, Microbial Ecology And Single Cell Analysis. Springer-Verlag, Berlin Heidelberg, 237-257.
18. Ducklow, H. W. 1994. Modeling the microbial food web. Microb. Ecol. 28:303-19.
19. Elbrächter, M., Hemleben, C. & Spindler, M. 1987. On the taxonomy of the lunate Pyrocytis species (Dinophyta). Bot. Mar. 30:233-41.
20. Elwood, H. J., Olen, G. J. & Sogin, M. L. 1985. The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol. Biol. Evol. 2: 399-410.
21. Estep, K. W., Davis, P. G., Hargraves, P. E. & Sieburth, J. M. 1984. Chloroplast containing microflagellates in natural populations of North Atlantic nanoplankton, their identification and distribution; including a description of five new species of Chrysochromulina (Prymnesiophyceae). Protistologica 20:613-34.
22. Fell, J. W. 1993. Rapid identification of yeast species using three primers in a polymerase chain reaction. Mol. Mar. Biol. Biotechnol. 2:174-80.
23. Fenchel, T. 1982a. Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol. Prog. Ser. 8:211-23.
24. _ 1982b. Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar. Ecol. Prog. Ser. 8:225-31.
25. _ 1982c. Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar. Ecol. Prog. Ser. 9:35-42.
26. Gast, R. J. & Caron, D. A. 1996. Molecular phylogeny of symbiotic dinoflagellates from Foraminifera and Radiolaria. Mol. Biol. Evol. 13:1192-7.
27. Goldman, J. C. & Caron, D. A. 1985. Experimental studies on an omnivorous microflagellate: implications for grazing and nutrient regeneration in the marine microbial food chain. Deep-Sea Res. 32:899-915.
28. Goldman, J. C., Caron, D. A., Andersen, O. K. & Dennett, M. R. 1985. Nutrient cycling in a microflagellate food chain: I. Nitrogen dynamics. Mar. Ecol. Prog. Ser. 24:231-42.
29. Hällfors, G. & Hällfors, S. 1988. Records of chrysophytes with siliceous scales (Mallomonadaceae and Paraphysomonadaceae) from Finnish inland waters. Hydrobiologia 161:1-19.
30. Hansen, P. 1996. Silica-scaled Chrysophyceae and Synurophyceae from Madagascar. Arch. Protistenkd. 147:145-72.
31. Hinkle, G. & Sogin, M. L. 1993. The evolution of the Vahlkampfiidae as deduced from 16S-like ribosomal RNA analysis. J. Eukaryot. Microbiol. 40:599-603.
32. Jacobson, D. M. & Anderson, D. M. 1986. Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J. Phycol. 22:249-58.
33. Joint, I. R., Owens, N. J. P. & Pomeroy, A. J. 1986. Seasonal production of photosynthetic picoplankton and nanoplankton in the Celtic Sea. Mar. Ecol Prog. Ser. 28:251-8.
34. Jones, R. I. 1994. Mixotrophy in planktonic protists as a spectrum of nutritional strategies. Mar. Microb. Food Webs 8:87-96.
35. Knauber, D. C., Berry, E. S. & Fawley, M. W. 1996. Ribosomal RNA-based oligonucleotide probes to identify marine green ultraphytoplankton. J. Eukaryot. Microbiol 43:89-94.
36. Kristiansen, J. & Andersen, R. A. [Eds.]. 1986. Chrysophytes: Aspects and Problems. Cambridge University Press, Cambridge, 337 pp.
37. Landry, M. R., Lehner-Fournier, J. M., Sundstrom, J. A., Fagerness, V. L. & Selph, K. E. 1991. Discrimination between living and heat-killed prey by a marine zooflagellate, Paraphysomonas vestita (Stokes). J. Exp. Mar. Biol. Ecol. 146:139-51.
38. Leadbeater, B. S. C. 1993. Preparation of pelagic protists for electron microscopy. In Kemp, P. F., Sherr, B. F., Sherr, E. B. & Cole, J. J. [Eds.] Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, pp. 241-251.
39. Leadbeater, B. S. C. & Barker, D. A. N. 1995. Biomineralization and scale production in the Chrysophyta. in Sandgren, C. D., Smol, J. P. & Kristiansen, J. [Eds.] Chrysophyte Algae: Ecology, Phylogeny and Development. Cambridge University Press, Cambridge, pp. 141-64.
40. Leipe, D. D., Wainright, P. O., Gunderson, J. H., Porter, D., Patterson, D. J., Valois, F., Himmerich, S. & Sogin, M. L. 1994. The stramenopiles from a molecular perspective: 16S-like rRNA sequences from Labyrinthuloides minuta and Cafeteria roenbergensis. Phycologia 33:369-77.
41. Lim, E. E., Amaral, L. A., Caron, D. A. & DeLong, E. F. 1993. Application of rRNA-based probes for observing marine nanoplanktonic protists. Appl. Environ. Microbiol. 59:1647-55.
42. Lim, E. L. 1997. New insights on the ecology of free-living, heterotrophic nanoflagellates based on the use of molecular biological approaches. Ph.D. thesis, Massachusetts Institute of Technology and Woods Hole Oceanographic Institution, Boston, MA, pp. 199.
43. Lim, E. L., Caron, D. A. & DeLong, E. F. 1996. Development and field application of a quantitative method for examining natural assemblages of protists using oligonucleotide probes. Appl. Environ. Microbiol. 62:1416-23.
44. Lim, E. L., Caron, D. A. & Dennett, M. R. 1999. The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in coastal water samples and enrichment culture. Limnol. Oceanogr. 44:37-51.
45. Malone, T. C. 1971. The relative importance of nannoplankton and netplankton as primary producers in tropical oceanic and neritic phytoplankton communities. Limnol. Oceanogr. 16: 633-9.
46. McLaughlin, G. L., Montenegrojames, S., Vodkin, M. H., et al. 1992. Molecular approaches to malaria and babesiosis diagnosis. Mem. Inst. Oswaldo Cruz 87:57-68.
47. 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.
48. Nicholls, K. H. 1989. Paraphysomonas caelifrica new to North America and an amended description of Paraphysomonas subrotacea (Chrysophyceae). Can. J. Bot. 67:2525-7.
49. Patterson, D. J. 1994. Protozoa: evolution and systematics. In Hausmann, K. & Hülsmann, N. [Eds.] Progress in Protozoology, Proceedings of the IX International Congress of Protozoology, Berlin 1993. Gustav Fischer Verlag, Stuttgart, pp. 1-14.
50. Peters, F., Choi, J. W. & Gross, T. 1996. Paraphysomonas imperforata (Protista, Chrysomonadida) under different turbulence levels: feeding, physiology and energetics. Mar. Ecol. Prog. Ser. 134:235-45.
51. Petrushevskaya, M. G. & Swanberg, N. R. 1990. Variability in skeletal morphology of colonial Radiolaria (Actinopoda: Polycystinea: Collosphaeridae). Micropaleontology 36:65-85.
52. Pick, F. R. & Caron, D. A. 1987. Picoplankton and nanoplankton biomass in Lake Ontario: relative contribution of phototrophic and heterotrophic communities. Can. J. Fish. Aquat. Sci. 44:2164-72.
53. Preisig, H. R. & Hibberd, D. J. 1982a. Ultrastructure and taxonomy of Paraphysomonas (Chrysophyceae) and related genera 1. Nord. J. Bot. 2:397-420.
54. _ 1982b. Ultrastructure and taxonomy of Paraphysomonas (Chrysophyceae) and related genera 2. Nord. J. Bot. 2:601-38.
55. _ 1983. Ultrastructure and taxonomy of Paraphysomonas (Chrysophyceae) and related genera 3. Nord. J. Bot. 3:695-723.
56. Rice, J., O'Connor, C. D., Sleigh, M. A., Burkill, P. H., Giles, I. G. & Zubkov, M. V. 1997a. Fluorescent oligonucleotide rDNA probes that specifically bind to a common nanoflagellate, Paraphysomonas vestita. Microbiology 143:1717-27.
57. Rice, J., Sleigh, M. A., Burkill, P. H., Tarran, G. A., O'Connor, C. D. & Zubkov, M. V. 1997b. Flow cytometric analysis of characteristics of hybridization of species-specific fluorescent oligonucleotide probes to rRNA of marine nanoflagellates. Appl. Environ. Microbiol. 63:938-944.
58. Saiki, R. K. e. a. 1988. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239:487-94.
59. Sambrook, J., Fritsch, E. F. & Maniatis, T. 1984. Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Plainview, New York.
60. Sandgren, C. D., Smol, J. P. & Kristiansen, J. [Eds.]. 1995. Chrysophyte Algae: Ecology, Phylogeny and Development. Cambridge University Press, Cambridge, 399 pp.
61. Saunders, G. W., Potter, D. & Andersen, R. A. 1997. Phylogenetic affinities of the Sarcinochrysidales and Chrysomeridales (Heterokonta) based on analyses of molecular and combined data. J. Phycol. 33:310-8.
62. Sherr, B. F., Sherr, E. B. & Paffenhöfer, G-A. 1986. Phagotrophic protozoa as food for metazoans: a "missing" trophic link in marine pelagic food webs. Mar. Microb. Food Webs 1:61-80.
63. Sherr, E. B., Caron, D. A. & Sherr, B. F. 1993. Staining of heterotrophic protists for visualization via epifluorescence microscopy. In Kemp, P., Cole, J., Sherr, B. & Sherr, E. [Eds.] Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, pp. 213-27.
64. Sherr, E. B. & Sherr, B. F. 1988. Role of microbes in pelagic food webs: a revised concept. Limnol. Oceanogr. 33:1225-7.
65. _ 1994. Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb. Ecol. 28:223-35.
66. Sieburth, J. M., Smetacek, V. & Lenz, J. 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr. 23:1256-63.
67. Simon, N., Brenner, J., Edvardsen, B. & Medlin, L. K. 1997. The identification of Chrysochromulina and Prymnesium species (Haptophyta, Prymnesiophyceae) using fluorescent or chemiluminescent oligonucleotides probes: a means for improving studies on toxic algae. Eur. J. Phycol. 32:393-401.
68. Sogin, M. L. & Gunderson, J. H. 1987. Structural diversity of eukaryotic small subunit ribosomal RNAs. Ann. N.Y. Acad. Sci. 503:125-39.
69. Stoecker, D. K. 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J. Protistol. 34:281-90.
70. Stoecker, D. K. & Capuzzo, J. M. 1990. Predation on protozoa: its importance to zooplankton. J. Plankton Res. 12:891-908.
71. Takahashi, E. 1976. Studies on genera Mallomonas and Synura, and other plankton in freshwater with the electron microscope X. The genus Paraphysomonas (Chrysophyceae) in Japan. Br. Phycol. J. 11:39-48.
72. Thomsen, H. A. 1975. An ultrastructural survey of the Chrysophycean genus Paraphysomonas under natural conditions. Br. Phycol. J. 10:113-27.
73. Turley, C. M. & Carstens, M. 1991. Pressure tolerance of oceanic flagellates: implications for remineralization of organic matter. Deep-Sea Res. 38:403-13.
74. Vørs, N. 1993. Heterotrophic amoebae, flagellates and heliozoa from Arctic marine waters (North West Territories, Canada and West Greenland). Polar Biol. 13:113-26.
75. Wehr, J. D. 1990. Predominance of picoplankton and nanoplankton in eutrophic Calder Lake. Hydrobiologia 203:35-44.
76. Wujek, D. E. & O'Kelly, C. J. 1992. Silica-scaled Chrysophyceae (Mallomonadaceae and Paraphysomonadaceae) from New Zealand freshwaters. N.Z.J. Bot. 30:405-14.
77. Wujek, D. E. & Saha, L. C. 1995. The genus Paraphysomonas from Indian rivers, lakes, ponds and tanks. In Sandgren, C. D., Smol, J. P. & Kristiansen, J. [Eds.] Chrysophyte Algae: Ecology, Phylogeny and Development. Cambridge University Press, Cambridge, pp. 373-84.