Chapter 5 : The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815509/9781555814069_Chap05-1.gif /docserver/preview/fulltext/10.1128/9781555815509/9781555814069_Chap05-2.gif


The development of improved preservation and staining techniques and particularly the application of electron microscopy provided a wealth of morphological information to improve the taxonomic criteria used for the description and identification of protists. This chapter concerns the "seen and unseen," "cultured and uncultured" protists, with a brief overview of these three categories. Ecological studies of cultured protists have included representatives from most of the major lineages of protists and have detailed the nutritional aspects of these species, their elemental stoichiometries, feeding behaviors and rates, growth rates, and growth efficiencies. The understanding of the biogeochemical significance and activities of these species has been ascertained largely through the manipulation and experimental examination of cultured protists. Using this information, ecologists have generated biogeochemical and food web models that significantly improved our understanding of the activities of photosynthetic and heterotrophic protists in natural communities and thus lend better insight into how aquatic communities function. The alveolates contain three well-known groups of protists: the ciliates, the dinoflagellates, and the apicomplexans. An example of the extensive genetic diversity detected in these very small protists can be found in the picoprasinophyte genus . Success in this work obviously requires some general knowledge of the nutrition of the target cells, so these attempts can improve dramatically as the "needs" of the protistan taxa are characterized.

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

One recent proposition for the evolutionary relationships among living eukaryotic organisms. Note that protistan taxa dominate the many eukaryotic lineages of organisms with respect to diversity and evolutionary breadth. From S. L. Baldauf, D. Bhattacharya, J. Cockrill, P. Hugenholtz, J. Pawlowski, and A. G. B. Simpson. The tree of life: an overview, p. 43–75. J. Cracraft and M. J. Donoghue (ed.), chapter 4. Oxford University Press, Oxford, United Kingdom, 2004.

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Examples of morphologically described and commonly cultured protists (“seen and cultured”) and morphologically described but uncultured protists (“seen but uncultured”). (A) Differential interference contrast micrograph of , a facultatively phototrophic/heterotrophic protist (from D. J. Patterson). species have been cultured for many years. (B) A phase-contrast micrograph of a symbiont bearing antarctic acantharian. Neither the host nor the symbionts have been cultured. (C) Dark-field photomicrograph of the planktonic foraminiferan, and its intracellular dinoflagellate symbionts. Planktonic foraminifera have never been cultured, the symbionts of () have been. (D) An antarctic tintinnid ciliate photographed using differential interference contrast microscopy. Tintinnids have been isolated and cultured from numerous marine ecosystems. (E) Scanning electron micrograph of , a cultured, red-tide dinoflagellate. (F) Light micrograph of an antarctic species of . Species of this genus have only recently been brought into laboratory culture (see text). (G) Phase-contrast micrograph of a lobose amoeba maintained in enrichment cultures. (H) Dark-field photomicrograph of several species of symbiont-bearing colonial radiolaria. Central capsules of the radiolaria are visible as small dots within the pseudopodial networks. Dinoflagellate symbionts give the capsules a yellowish green color. The dinoflagellate symbiont, , has been cultured, but the hosts have never been. (I) Phase-contrast micrograph of , a cultured prymnesiophyte alga that forms mucilaginous colonies. Individual cells are the small dots embedded in the colony matrix. (J) sp., a heterotrophic dinoflagellate with episymbiotic cyanobacteria, visualized using phase-contrast microscopy. The host has not been cultured, but the cyanobacterium has. (K) Negatively stained, transmission electron micrograph of sp., a cultured antarctic prasinophyte. (L) Phase micrograph of sp., an antarctic diatom. (M) Phaselight micrograph of an unknown, uncultured antarctic diatom. (N) Light micrograph of the heterotrophic ebriid, sp. Ebriids have not been cultured. (O) The commonly cultured ciliate, , with ingested prey (the pelagophyte alga, ), photographed using light microscopy. The pelagophyte has also been cultured and can be used to maintain cultures of this ciliate. Marker bars are 20 μm (A, B, F, L), 300 μm (C, H), 40 μm (D, E, I, M), 10 μm (G, J, N, O), and 2 μm (K).

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3

(A) Rank-abundance curve of microbial taxa in an idealized microbial (bacterial) community and (B) an actual rank-abundance curve for a natural protistan assemblage. The inset in panel B shows an enlargement of the rank-abundance curve for the most commonly encountered phylotypes. Panel A is from ; panel B is from .

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4

A proposed phylogenetic tree indicating the placement of major clades of “undescribed, uncultured” protistan taxa within the alveolates. Taken from Groisellier et al., 2006.

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5

A proposed phylogenetic tree noting the association of several novel protistan clades within parasitic protistan lineages. Taken from .

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6

A proposed phylogenetic tree showing the placement of numerous novel marine stramenopile (MAST) phylotypes. Taken from .

Citation: Caron D, Gast R. 2008. The Diversity of Free-Living Protists Seen and Unseen, Cultured and Uncultured, p 67-93. In Zengler K (ed), Accessing Uncultivated Microorganisms. ASM Press, Washington, DC. doi: 10.1128/9781555815509.ch5
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Adl, S. M.,, A. G. B. Simpson,, M. A. Farmer,, R. A. Andersen,, O. R. Anderson,, J. R. Barta,, S. S. Bowser,, G. Brugerolle,, R. A. Fensome,, S. Fred-ericq,, T. Y. James,, S. Karpov,, P. Kugrens,, J. Krug,, C. E. Lane,, L. A. Lewis,, J. Lodge,, D. H. Lynn,, D. G. Mann,, R. M. McCourt,, L. Mendoza,, O. Moestrup,, S. E. Mozley-Standridge,, T. Nerad,, C. A. Shearer,, A. V. Smirnov,, F. W. Spiegel, and, M. F. J. R. Taylor. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Euk. Microbiol. 52:399451.
2. Amaral Zettler, L. A.,, M. A. Messerli,, A. D. Laatsch,, P. J. S. Smith, and, M. L. Sogin. 2003. From genes to genomes: beyond biodiversity in Spain’s Rio Tinto. Biol. Bull. 204:205209.
3. Andersen, O. K.,, J. C. Goldman,, D. A. Caron, and, M. R. Dennett. 1986. Nutrient cycling in a microflagellate food chain: III. Phosphorus dynamics. Mar. Ecol. Prog. Ser. 31:4755.
4. Andersen, R. A.,, G. W. Saunders,, M. P. Paskind, and, J. P. Sexton. 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. 29:701715.
5. Anderson, D. M.,, and J. S. Ramsdell. 2005. HARRNESS: a framework for HAB research and monitoring in the United States for the next decade. Oceanography 18:238245.
6. Anderson, O. R. 1980. Radiolaria, p. 1–42. In M. Levandowsky and, S. H. Hutner (ed.), Biochemistry and Physiology of Protozoa, vol. 3. Academic Press, New York, NY.
7. Armbrust, E. V.,, J. A. Berges,, C. Bowler,, B. R. Green,, D. Martinez,, N. H. Putnam,, S. G. Zhou,, A. E. Allen,, K. E. Apt,, M. Bechner,, M. A. Brzezinski,, B. K. Chaal,, A. Chiovitti,, A. K. Davis,, M. S. Demarest,, J. C. Detter,, T. Glavina,, D. Goodstein,, M. Z. Hadi,, U. Hellsten,, M. Hildebrand,, B. D. Jenkins,, J. Jurka,, V. V. Kapitonov,, N. Kroger,, W. W. Y. Lau,, T. W. Lane,, F. W. Larimer,, J. C. Lippmeier,, S. Lucas,, M. Medina,, A. Montsant,, M. Obornik,, M. S. Parker,, B. Palenik,, G. J. Pazour,, P. M. Richardson,, T. A. Rynearson,, M. A. Saito,, D. C. Schwartz,, K. Thamatrakoln,, K. Valentin,, A. Vardi,, F. P. Wilkerson, and, D. S. Rokhsar. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:7986.
8. Baldauf, S. L. 2003. The deep roots of eukaryotes. Science 300:17031706.
9. Baldauf, S. L.,, A. J. Roger,, I. Wenk-Siefert, and, W. F. Doolittle. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972977.
10. Bé, A. W. H.,, O. R. Anderson,, W. W. Faber, Jr., and, D. A. Caron. 1983. Sequence of morphological and cytoplasmic changes during gametogenesis in the planktonic foraminifer Globigerinoides sacculifer (Brady). Micropaleontology 29:310325.
11. Bé, A. W. H.,, H. J. Spero, and, O. R. Anderson. 1982. Effects of symbiont elimination and reinfection on the life processes of the planktonic foraminifer Globigerinoides sacculifer. Mar. Biol. 70:7386.
12. Berney, C.,, J. Fahrni, and, J. Pawlowski. 2004. How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of environmental DNA surveys. BMC Biol. 4:213.
13. Boenigk, J.,, S. Jost,, T. Stoeck, and, T. Garstecki. 2006. Differential thermal adaptation of clonal strains of a protist morphospecies originating from different climatic zones. Environ. Microbiol. 9:593602.
14. Boenigk, J.,, K. Pfandl,, P. Stadler, and, A. Chatzinotas. 2005. High diversity of the “Spumella-like” flagellates: an investigation based on the SSU rRNA gene sequences of isolates from habitats located in six different geographic regions. Environ. Microbiol. 7:685697.
15. Bolch, C. J. S. 2001. PCR protocols for genetic identification of dinoflagellates directly from single cysts and plankton cells. Phycologia 40:162167.
16. Buckley, M.,, and R. J. Roberts. 2007. Reconciling microbial systematics and genomics. American Academy of Microbiology, Washington, D. C.
17. Calbet, A.,, and M. R. Landry. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:5157.
18. Calkins, G. N. 1901. Marine protozoa from Woods Hole. Bull. Bur. Fish. 21:413468.
19. Caron, D. A.,, J. C. Goldman,, O. K. Andersen, and, M. R. Dennett. 1985. Nutrient cycling in a microflagellate food chain. II. Population dynamics and carbon cycling. Mar. Ecol. Prog. Ser. 24:243254.
20. Caron, D. A.,, E. L. Lim,, H. Kunze,, E. M. Cosper, and, D. M. Anderson. 1989. Trophic interactions between nano- and microzooplankton and the “brown tide,” p. 265–294. In E. M. Cosper,, V. M. Bricelj, and, E. J. Carpenter (ed.), Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and Other Unusual Blooms, vol. 35. Springer-Verlag, Berlin, Germany.
21. Caron, D. A.,, A. F. Michaels,, N. R. Swanberg, and, F. A. Howse. 1995. Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J. Plankton Res. 17:103129.
22. Caron, D. A.,, and N. R. Swanberg. 1990. The ecology of planktonic sarcodines. Rev. Aquat. Sci. 3:147180.
23. Carvalho, W. F.,, and E. Graneli. 2006. Acidotropic probes and flow cytometry: a powerful combination for detecting phagotrophy in mixotrophic and heterotrophic protists. Aquat. Microb. Ecol. 44:8596.
24. Cavalier-Smith, T. 1998. A revised six-kingdom system of life. Biol. Rev. 73:203266.
25. Choi, J. W.,, and F. Peters. 1992. Effects of temperature on two psychrophilic ecotypes of a heterotrophic nanoflagellate, Paraphysomonas imperforata. Appl. Environ. Microbiol. 58:593599.
26. Coats, D. W.,, E. J. Adam,, C. L. Gallegos, and, S. Hedrick. 1996. Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA. Aquat. Microb. Ecol. 11:19.
27. Coats, D. W.,, and M. G. Park. 2002. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya ( Dinophyta):parasite survival, infectivity, generation time, and host specificity. J. Phycol. 38:520528.
28. Countway, P. D.,, R. J. Gast,, M. R. Dennett,, P. Savai,, J. M. Rose, and, D. A. Caron. 2007. Distinct protistan assemblages characterize the euphotic zone and deep sea (2500 m) of the western N. Atlantic (Sargasso Sea and Gulf Stream). Environ. Microbiol. 9:12191232.
29. Courties, C.,, A. Vaquer,, M. Troussellier,, J. Lautier,, M. Chretiennot-Dinet,, J. Neveux,, C. Machado, and, H. Claustre. 1994. Smallest eukaryotic organism. Nature 370:255.
30. Crawford, D. W. 1989. Mesodinium rubrum: the phytoplankter that wasn’t. Mar. Ecol. Prog. Ser. 58:161174.
31. Croft, M. T.,, M. J. Warren, and, A. G. Smith. 2006. Algae need their vitamins. Eukaryotic Cell 5:11751183.
32. Daniels, R. B.,, T. L. Richardson, and, H. W. Duck-low. 2006. Food web structure and biogeochemical processes during oceanic phytoplankton blooms: an inverse model analysis. Deep-Sea Res. 53:532554.
33. Dawson, S. C.,, and N. R. Pace. 2002. Novel kingdom-level eukaryotic diversity in anoxic environments. Proc. Natl. Acad. Sci. USA 99:83248329.
34. DeLong, E. F. 2004. Microbial population genomics and ecology: the road ahead. Environ. Microbiol. 6:875878.
35. Dolven, J. K.,, C. Lindqvist,, V. A. Albert,, K. R. Bjørklund,, T. Yuasa,, O. Takahashi, and, S. Mayama. 2007. Molecular diversity of alveolates associated with neritic North Atlantic radiolarians. Protist 158:6576.
36. Edgcomb, V. P.,, D. T. Kysela,, A. Teske,, A. D. Gomez, and, M. L. Sogin. 2002. Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc. Natl. Acad. Sci. USA 99:76587662.
37. Edvardsen, B.,, K. Shalchian-Tabrizi,, K. S. Jakobsen,, L. Medlin,, K., E. Dahl,, S. Brubak, and, E. Paasche. 2003. Genetic variability and molecular phylogeny of Dinophysis species (Dinophyceae) from Norwegian waters inferred from single cell analyses of rDNA. J. Phycol. 39:395408.
38. Falkowski, P. G.,, and J. Raven. 1997. Aquatic Photosynthesis. Blackwell Scientific, Oxford, United Kingdom.
39. Fauré-Fremiet, E. 1924. Contribution à la connaissance des infusoires planktoniques. Bull. Biol. France Belgique (Suppl) 6:1171.
40. Fawley, M. J.,, K. P. Fawley, and, M. A. Buchheim. 2004. Molecular diversity among communities of freshwater microchlorophytes. Microb. Ecol. 48:489499.
41. Fawley, M. W.,, K. P. Fawley, and, H. A. Owen. 2005. Diversity and ecology of small coccoid green algae from Lake Itasca, Minnesota, USA, including Meyerella planktonica, gen. et sp nov. Phycologia 44:3548.
42. Fenchel, T. 1982a. Ecology of heterotrophic microflagellates. I. Some important forms and their functional morphology. Mar. Ecol. Prog. Ser. 8:211223.
43. Fenchel, T. 1982b. Ecology of heterotrophic microflagellates. III. Adaptations to heterogeneous environments. Mar. Ecol. Prog. Ser. 9:2533.
44. Finlay, B. J. 2002. Global dispersal of free-living microbial eukaryote species. Science 296:10611063.
45. Finlay, B. J.,, and K. J. Clarke. 1999. Apparent global ubiquity of species in the protist genus Paraphysomonas. Protist 150:419430.
46. Finlay, B. J.,, and T. Fenchel. 1999. Divergent perspectives on protist species richness. Protist 150:229233.
47. Foissner, W. 1999. Protist diversity: estimates of the near-imponderable. Protist 72:65786583.
48. Gast, R. J. 2006. Molecular phylogeny of a potentially parasitic dinoflagellate isolated from the solitary radiolarian, Thalassicolla nucleata. J. Euk. Microbiol. 53:4345.
49. Gast, R. J.,, M. R. Dennett, and, D. A. Caron. 2004. Characterization of protistan assemblages in the Ross Sea, Antarctica by denaturing gradient gel electrophoresis. Appl. Environ. Microbiol. 70:20282037.
50. Gast, R. J.,, D. M. Moran,, M. R. Dennett, and, D. A. Caron. 2007. Kleptoplasty in an Antarctic dinoflagellate: caught in evolutionary transition? Environ. Microbiol. 9:3945.
51. Girvan, M. S.,, C. D. Campbell,, K. Killham,, J. I. Prosser, and, L. A. Glover. 2005. Bacterial diversity promotes community stability and functional resilience after perturbation. Environ. Microbiol. 7:301313.
52. Goldman, J. C.,, and D. A. Caron. 1985. Experimental studies on an omnivorous microflagellate: implications for grazing and nutrient regeneration in the marine microbial food chain. Deep-Sea Res. 32:899915.
53. Goldman, J. C.,, D. A. Caron,, O. K. Andersen, and, M. R. Dennett. 1985. Nutrient cycling in a microflagellate food chain: I. Nitrogen dynamics. Mar. Ecol. Prog. Ser. 24:231242.
54. Gordon, N.,, D. L. Angel,, A. Neori,, N. Kress, and, B. Kimor. 1994. Heterotrophic dinoflagellates with symbiotic cyanobacteria and nitrogen limitation in the Gulf of Aqaba. Mar. Ecol. Prog. Ser. 107:8388.
55. Gran, H. H. 1912. Pelagic plant life, p. 307–386. In J. Murray and, J. Hjort (ed.), The Depths of the Ocean. MacMillan, London, United Kingdom.
56. Griffiths, B. S.,, H. L. Kuan,, K. Ritz,, L. A. Glover,, A. E. McCaig, and, C. Fenwick. 2004. The relationship between microbial community structure and functional stability, tested experimentally in an upland pasture soil. Microb. Ecol. 47:104113.
57. Groisillier, A.,, R. Massana,, K. Valentin,, D. Vaulot, and, L. Guillou. 2006. Genetic diversity and habitats of two enigmatic marine alveolate lineages. Aquat. Microb. Ecol. 42:277291.
58. Gruebl, T.,, M. E. Frischer,, M. Sheppard,, M. Neumann,, A. N. Maurer, and, R. F. Lee. 2002. Development of an 18S rRNA gene-targeted diagnostic for the blue crab parastie Hematodinium sp. Dis. Aquat. Org. 49:6170.
59. Guillou, L.,, M.- J. Chrétiennot-Dinet,, L. K. Medlin,, H. Claustre,, S. Loiseaux-de Goer, and, D. Vaulot. 1999a. Bolidomonas: a new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). J. Phycol. 35:368381.
60. Guillou, L.,, W. Eikrem,, M. J. Chretiennot-Dinet,, F. Le Gall,, R. Massana,, K. Romari,, C. Pedros-Alio, and, D. Vaulot. 2004. Diversity of picoplank-tonic prasinophytes assessed by direct nuclear SSU rDNA sequencing of environmental samples and novel isolates retrieved from oceanic and coastal marine ecosystems. Protist 155:193214.
61. Guillou, L. R.,, M.- J. Chrétiennot-Dinet,, S. Boulben,, S. Y. Moon-van der Staay, and, D. Vaulot. 1999b. Symbiomonas scintillans gen. et sp. nov. and Picophagus flagellatus gen. et sp. nov. (Heterokonta): two new heterotrophic flagellates of picoplanktonic size. Protist 150:383398.
62. Hackett, J. D.,, D. M. Anderson,, D. L. Erdner, and, D. Bhattacharya. 2004. Dinoflagellates: a remarkable evolutionary experiment. Am. J. Bot. 91:15231534.
63. Haeckel, E. 1887. Report on Radiolaria collected by H. M. S. Challenger during the 1873–1876, p. 1–1760. In C. W. Thompson and, J. Murray (ed.), The Voyage of the H. M. S. Challenger, vol. 18. Her Majesty’s Stationary Office, London, United Kingdom.
64. Hausmann, K.,, and N. Hülsmann. 1996. Protozoology. Georg Thieme Verlag, Stuttgart, Germany.
65. Hemleben, C.,, M. Spindler, and, O. R. Anderson. 1988. Modern Planktonic Foraminifera. Springer-Verlag, New York, NY.
66. Hill, H. Z.,, H. T. Epstein, and, J. A. Schiff. 1966. Studies of chloroplast development in euglena. XIV. Sequential interactions of ultraviolet light and photoreactivating light in green colony formation. Biophys. J. 6:135144.
67. Holzmann, M.,, A. Habura,, H. Giles,, S. S. Bowser, and, J. Pawlowski. 2003. Freshwater foraminiferans revealed by analysis of environmental DNA samples. J. Euk. Microbiol. 50:135139.
68. Hoppenrath, M.,, and B. S. Leander. 2006. Ebriid phylogeny and the expansion of the Cercozoa. Protist 157:279290.
69. Jeon, S.-O.,, J. Bunge,, T. Stoeck,, K. J.-A. Barger,, S.- H. Hong, and, S. S. Epstein. 2006. Synthetic statistical approach reveals a high degree of richness of microbial eukaryotes in an anoxic water column. Appl. Environ. Microbiol. 72:65786583.
70. Jeong, H. J. 1999. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Euk. Microbiol. 46:390396.
71. Jeong, H. J.,, Y. D. Yoo,, J. Y. Park,, J. Y. Song,, S. T. Kim,, S. H. Lee,, K. Y. Kim, and, W. H. Yih. 2005. Feeding by red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic. Aquat. Microb. Ecol. 40:133150.
72. Johnson, M. D.,, D. Oldach,, D. F. Delwiche, and, D. K. Stoecker. 2007. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426428.
73. Karpov, S. A.,, D. Bass,, A. P. Mylnikov, and, T. Cavalier-Smith. 2006. Molecular phylogeny of Cercomonadidae and kinetid patterns of Cercomonas and Eocercomonas gen. nov. (Cercomonadida, Cercozoa). Protist 157:125158.
74. Kawachi, M.,, M. Atsumi,, H. Ikemoto, and, S. Miyachi. 2002. Pinguiochrysis pyriformis gen. et sp. nov. (Pinguiophyceae), a new picoplanktonic alga isolated from the Pacific Ocean. Phycol. Res. 50:4956.
75. Ki, J.-S.,, G. Y. Jang, and, M.- S. Han. 2004. Integrated method for single-cell DNA extraction, PCR amplification and sequencing of ribosomal DNA from harmful dinoflagellates Cochlodinium polykrikoides and Alexandrium catenella. Mar. Biotechnol. 6:587593.
76. Kofoid, C. A.,, and T. Skogsberg. 1928. The free-living unarmoured dinoflagellates. Mem. Univ. California, Berkeley 5:563.
77. Kolodziej, K.,, and T. Stoeck. 2007. Cellular identification of a novel uncultured marine stramenopile (MAST-12 Clade) small-subunit rRNA gene sequence from a Norwegian estuary by use of fluorescence in situ hybridization-scanning electron microscopy. Appl. Environ. Microbiol. 73:27182726.
78. Lee, J. J.,, and O. R. Anderson (ed.). 1991. The Biology of Foraminifera. Academic Press, London, United Kingdom.
79. Lee, J. J.,, S. H. Hutner, and, E. C. Bovee (ed.). 1985. An Illustrated Guide to the Protozoa. Society of Protozoologists, Lawrence, KS.
80. Lee, J. J.,, G. F. Leedale, and, P. Bradbury. 2000. An Illustrated Guide to the Protozoa. Allen Press, Inc., Lawrence, KS.
81. Lee, J. J.,, C. W. Reimer, and, M. E. McEnery. 1980. The identification of diatoms isolated as endosymbionts from larger foraminifera from the Gulf of Eilat (Red Sea) and the description of 2 new species, Fragilaria shiloi sp. nov. and Navicula reissii sp. nov. Botanica Marina 23:4148.
82. Lee, J. J.,, K. Sang,, B. ter Kuile,, E. Strauss,, P. J. Lee, and, W. W. Faber, Jr. 1991. Nutritional and related experiments on laboratory maintenance of three species of symbiont-bearing, large foraminifera. Mar. Biol. 109:417425.
83. Leidy, J. 1879. Fresh-water rhizopods of North America. U. S. Geological Survey of the Territories 12:1234.
84. Lessard, E. J. 1991. The trophic role of heterotrophic dinoflagellates in diverse marine environments. Mar. Microb. Food Webs 5:4958.
85. Lim, E. E.,, L. A. Amaral,, D. A. Caron, and, E. F. DeLong. 1993. Application of rRNA-based probes for observing marine nanoplanktonic protists. Appl. Environ. Microbiol. 59:16471655.
86. Lim, E. L.,, D. A. Caron, and, M. R. Dennett. 1999. The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in coastal water samples and enrichment culture. Limnol. Oceanogr. 44:3751.
87. Lohmann, H. 1902. Die Coccolithophoridae, eine Monographie der coccolithen bildenden Flagellaten. Arch. Prot. 1:89165.
88. López-García, P.,, A. Lopez-Lopez,, D. Moreira, and, F. Rodríguez-Valera. 2001a. Diversity of free-living prokaryotes from a deep-sea site at the Antarctic Polar Front. FEMS Microbiol. Ecol. 36:193202.
89. López-García, P.,, F. Rodríguez-Valera,, C. Pedrós-Alió, and, D. Moreira. 2001b. Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603607.
90. López-Garcia, P.,, A. Vereshchaka, and, D. Moreira. 2007. Eukaryotic diversity associated with carbonates and fluid-seawater interface in Lost City hydrothermal field. Environ. Microbiol. 9:546554.
91. Lovejoy, C.,, R. Massana, and, C. Pedros-Alio. 2006. Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent seas. Appl. Environ. Microbiol. 72:30853095.
92. Lovejoy, C.,, W. F. Vincent,, S. Bonilla,, S. Roy,, M.- J. Martineau,, R. Terrado,, M. Potvin,, R. Massana, and, C. Pedrós-Alió. 2007. Distribution, phylogeny and growth of cold-adapted picoprasinophytes in Arctic Seas. J. Phycol. 43:7889.
93. Luo, Q.,, L. R. Krumholz,, F. Z. Najar,, A. D. Peacock,, B. A. Roe,, D. C. White, and, M. S. Elshahed. 2005. Diversity of the microeukaryotic community in sulfide-rich Zodletone Spring (Oklahoma). Appl. Environ. Microbiol. 71:61756184.
94. Massana, R.,, V. Balagué,, L. Guillou, and, C. Pedrós-Alió. 2004. Picoeukaryotic diversity in an oligotrophic coastal site studied by molecular and culturing approaches. FEMS Microbiol. Ecol. 50:231243.
95. Massana, R.,, J. Castresana,, V. Balagué,, L. Guillou,, K. Romari,, A. Groisillier,, K. Valentin, and, C. Pedrós-Alió. 2004. Phylogenetic and ecological analysis of novel marine stramenopiles. Appl. Environ. Microbiol. 70:35283534.
96. Massana, R.,, L. Guillou,, B. Diez, and, C. Pedros-Alio. 2002. Unveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean. Appl. Environ. Microbiol. 68:45544558.
97. Massana, R.,, L. Guillou,, R. Terrado,, I. Forn, and, C. Pedrós-Alió. 2006a. Growth of uncultured heterotrophic flagellates in unamended seawater incubations. Aquat. Microb. Ecol. 45:171180.
98. Massana, R.,, R. Terrado,, I. Form,, C. Lovejoy, and, C. Pedrós-Alió. 2006b. Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ. Microbiol. 8:15151522.
99. McGrady-Steed, J.,, P. M. Harris, and, P. J. Morin. 1997. Biodiversity regulates ecosystem predictability. Nature 390:162165.
100. Michaels, A. F.,, D. A. Caron,, N. R. Swanberg,, F. A. Howse, and, C. M. Michaels. 1995. Planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda: abundance, biomass and vertical flux. J. Plankton Res. 17:131163.
101. Modeo, L.,, G. Petroni,, G. Rosati, and, D. J. S. Montagnes. 2003. A multidisciplinary approach to describe protists: redescriptions of Novistrombidium testaceum and Strombidium inclinatum Montagnes, Taylor and Lynn 1990 (Ciliophora, Oligotrichia). J. Euk. Microbiol. 50:175189.
102. Moon-van der Staay, S. Y.,, R. De Wachter, and, D. Vaulot. 2001. Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity. Nature 409:607610.
103. Moreira, D.,, and P. Lopez-Garcia. 2003. Are hydrothermal vents oases for parasitic protists? Trends Parasitol. 19:556558.
104. Naeem, S.,, and L. Shibin. 1997. Biodiversity enhances ecosystem stability. Nature 390:507509.
105. Not, F.,, K. Valentin,, K. Romari,, C. Lovejoy,, R. Massana,, K. Töbe,, D. Vaulot, and, L. K. Medlin. 2007. Picobiliphytes: a marine picoplanktonic algal group with unknown affinities to other eukaryotes. Science 315:253255.
106. Okamoto, N.,, and I. Inouye. 2007. A secondary symbiosis in progress. Science 310:287.
107. Park, M. G.,, S. K. Cooney,, J. S. Kim, and, D. W. Coats. 2002a. Effects of parasitism on diel vertical migration, phototaxis/geotaxis, and swimming speed of the bloom-forming dinoflagellate Akashiwo sanguinea. Aquat. Microb. Ecol. 29:1118.
108. Park, M. G.,, S. K. Cooney,, W. Yih, and, D. W. Coats. 2002b. Effects of two strains of the parastic dinoflagellate Amoebophrys on growth, photosynthesis, light absorption, and quantum yield of bloom-forming dinoflagellates. Mar. Ecol. Prog. Ser. 227:281292.
109. Park, M. G.,, S. Kim,, H. S. Kim,, G. Myung,, Y. G. Kang, and, W. Yih. 2006. First successful culture of the marine dinoflagellate Dinophysis. Aquat. Microb. Ecol. 45:101106.
110. Park, M. G.,, W. Yi, and, D. W. Coats. 2004. Parasites and phytoplankton, with special emphasis on dinoflagellate infections. J. Euk. Microbiol. 51:145155.
111. Patterson, D. J. 1999. The diversity of eukaryotes. Am. Nat. 154 (Suppl):S96S124.
112. Patterson, D. J.,, and J. Larsen (ed.). 1991. The Biology of Free-Living Heterotrophic Flagellates. Clarendon Press, Oxford, United Kingdom.
113. Pedrós-Alió, C. 2006. Microbial diversity: can it be determined? Trends Microbiol. 14:257263.
114. Peters, F.,, J. W. Choi, and, T. Gross. 1996. Paraphysomonas imperforata (Protista, Chrysomonadida) under different turbulence levels: feeding, physiology and energetics. Mar. Ecol. Prog. Ser. 134:235245.
115. Podar, M.,, C. B. Abulencia,, M. Walcher,, D. Hutchinson,, K. Zengler,, J. A. Garcia,, T. Holland,, D. Cotton,, L. Hauser, and, M. Keller. 2007. Targeted access to the genomes of low-abundance organisms in complex microbial communities. Appl. Environ. Microbiol. 73:32053214.
116. Potter, D.,, T. C. LaJeunesse,, G. W. Saunders, and, R. A. Andersen. 1997. Convergent evolution masks extensive biodiversity among marine coccoid picoplankton. Biodivers. Conserv. 9:99107.
117. Raghunathan, A.,, H. R. Ferguson, Jr.,, C. J. Bornarth,, W. Song,, M. Driscoll, and, R. S. Lasken. 2005. Genomic DNA amplification from a single bacterium. Appl. Environ. Microbiol. 71:33423347.
118. Richardson, T. L.,, G. A. Jackson,, H. W. Ducklow, and, M. R. Roman. 2006. Spatial and seasonal patterns of carbon cycling through planktonic food webs of the Arabian Sea determined by inverse analysis. Deep-Sea Res. 534:555575.
119. Robbens, S.,, B. Khadaroo,, A. Camasses,, E. Derelle,, C. Ferraz,, D. Inze,, Y. van de Peer, and, H. Moreau. 2005. Genome-wide analysis of core cell cycle genes in the unicellular green alga Ostreococcus tauri. Mol. Biol. Evol. 22:589597.
120. Romari, K., and, D. Vaulot. 2004. Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences. Limnol. Oceanogr. 49:784798.
121. Rose, J. M.,, and D. A. Caron. 2007. Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold water. Limnol. Oceanogr. 52:886895.
122. Ruiz Sebastian, C.,, and C. O’Ryan. 2001. Single-cell sequencing of dinoflagellate (Dinophyceae) nuclear ribosomal genes. Molec. Ecol. Notes 1:329331.
123. Sanders, R. W.,, D. A. Caron, and, U.- G. Berninger. 1992. Relationships between bacteria and heterotrophic nanoplankton in marine and fresh water: an inter-ecosystem comparison. Mar. Ecol. Prog. Ser. 86:114.
124. Sanders, R. W.,, and K. G. Porter. 1988. Phagotrophic phytoflagellates. Adv. Microb. Ecol. 10:167192.
125. Scala, S.,, N. Carels,, A. Falciatore,, M. L. Chiusano, and, C. Bowler. 2002. Genome properties of the diatom Phaeodactylum tricornutum. Plant Physiol. 129:9931002.
126. Schewiakoff, W. 1926. Die Acantharia des Golfes von Neapel, p. 1–755. In G. Bardi (ed.), Fauna e Flora del Golfo di Napoli, vol. 37. R Friedlander und Sohn, Berlin, Germany.
127. Schlegel, M. 1994. Molecular phylogeny of eukaryotes. Trends Ecol. Evol. 9:330335.
128. Schlegel, M. 1991. Protist evolution and phylogeny as discerned from small subunit ribosomal RNA sequence comparisons. Eur. J. Protistol. 27:207219.
129. Schloss, P. D.,, and J. Handelsman. 2004. Status of the microbial census. Microbiol. Mol. Biol. Rev. 68:686691.
130. Schnepf, E.,, and M. Elbrächter. 1992. Nutritional strategies in dinoflagellates. Eur. J. Protistol. 28:324.
131. Shalchian-Tabrizi, K.,, W. Eikrem,, D. Klaveness,, D. Vaulot,, M. A. Minge,, F. LaGall,, K. Romari,, J. Throndsen,, A. Botnen,, R. Massana,, H. A. Thomsen, and, K. S. Jakobsen. 2006. Telonemia, a new protist phylym with affinity to chromist lineages. Proc. R. Soc. London, Ser. B 273:18331842.
132. Shalchian-Tabrizi, K.,, H. Kauserud,, R. Massana,, D. Klaveness, and, K. S. Jakobsen. 2007. Analysis of enviornmental 18S ribosomal RNA sequences reveals unknown diversity of the cosmopolitan phylum Telonemia. Protist 158:173180.
133. Sherr, B. F.,, E. B. Sherr,, D. A. Caron,, D. Vaulot, and, A. Z. Worden. 2007. Oceanic protists. Oceanography 20:102106.
134. Sherr, E. B.,, and B. F. Sherr. 2002. Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81:293308.
135. Simpson, A. G. B.,, and A. J. Roger. 2004. The real ‘kingdoms’ of eukaryotes. Curr. Biol. 14: R693696.
136. Slapeta, J.,, P. López-Garcia, and, D. Moreíra. 2006a. Global dispersal and ancient cryptic species in the smallest marine eukaryotes. Mol. Biol. Evol. 23:2329.
137. Slapeta, J. R.,, D. Moreira, and, P. López-García. 2006b. Present status of the molecular ecology of Kathablepharids. Protist 157:711.
138. Sogin, M. L.,, H. G. Morrison,, J. A. Huber,, D. M. Welch,, S. M. Huse,, P. R. Neal,, J. M. Arrieta, and, G. J. Herndl. 2006. Microbial diversity in the deep sea and the underexplored “rare biosphere.” Proc. Natl. Acad. Sci. USA 103:1211512120.
139. Stoeck, T.,, and S. Epstein. 2003. Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl. Environ. Microbiol. 69:26572663.
140. Stoeck, T.,, B. Hayward,, G. T. Taylor,, R. Varela, and, S. S. Epstein. 2006. A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:3143.
141. Stoeck, T.,, G. T. Taylor, and, S. S. Epstein. 2003. Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Appl. Environ. Microbiol. 69:56565663.
142. Stoeck, T.,, A. Zuendorf,, A. Behnke, and, H.- W. Breiner. 2007. A molecular approach to identify active microbes in environmental eukaryote clone libraries. Microb. Ecol. 53:328339.
143. Stoecker, D. K. 1999. Mixotrophy among dinoflagellates. J. Euk. Microbiol. 46:397401.
144. Stoecker, D. K.,, M. Putt,, L. H. Davis, and, A. E. Michaels. 1991. Photosynthesis in Mesodinium rubrum: species: specific measurements and comparison to community rates. Mar. Ecol. Prog. Ser. 73:245252.
145. Stoecker, D. K.,, M. W. Silver,, A. E. Michaels, and, L. H. Davis. 1989. Enslavement of algal chloroplasts by four Strombidium spp. (Ciliophora, Oligotrichida). Mar. Microb. Food Webs 3:79100.
146. Stokes, A. C. 1878. Der Organismus der Infusionthiere, vol. 3. W. Englemann, Leipzig, Germany.
147. Swanberg, N. R.,, and G. R. Harbison. 1980. The ecology of Collozoum longiforme, sp. nov., a new colonial radiolarian from the equatorial Atlantic Ocean. Deep-Sea Res. 27A:715732.
148. Takano, Y.,, and T. Horiguchi. 2005. Acquiring scanning electron microscopical, light microscopical and multiple gene sequence data from a single dinoflagellate cell. J. Phycol. 42:251256.
149. Takishita, K.,, H. Miyake,, M. Kawato, and, T. Maruyama. 2005. Genetic diversity of microbial eukaryotes in anoxic sediment around fumaroles on a submarine caldera floor based on the small-subunit rDNA phylogeny. Extremophiles 9:185196.
150. Yuasa, T.,, O. Takahashi,, J. K. Dolven,, S. Mayama,, A. Matsuoka,, D. Honda, and, K. R. Bjorklund. 2006. Phylogenetic position of the small solitary phaeodarians (Radiolaria) based on 18S rDNA sequences by single cell PCR analysis. Mar. Micropaleontol. 59:104114.
151. Zaslavskaia, L. A.,, J. C. Lippmeier,, P. G. Kroth,, K. E. Apt, and, A. R. Grossman. 2000. Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of detectable marker and reporter genes. J. Phycol. 36:379386.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error