sign in sign up
<<
Home , Heterotrophic nutrition, Marine protists, Picoeukaryote

or collective redistirbution other or collective or means this reposting, of machine, is bySociety, photocopy article only anypermitted of withSociety. Send portion theall Box 1931, R PO approvalOceanographycorrespondence Oceanography to: [email protected] The of or Th e This article has been published in published been This has article A s e a of M i c r ob e s

> Section V. Ex amples of Diversit y

> Chapter 10. Microbial Communities Oceanography > A . Water Column Oceanic , VolumeSociety.Society. 2, a quarterlyOceanography 20, Number The A journalCopyrightOceanography of 2007 by The By Barry F. Sherr, Evelyn B. Sherr, David A. Caron, Daniel Vaulot, and Alexandra Z. Worden

Protists are microscopic eukaryotic form massive blooms that can be seen organisms for . Most are phago- microbes that are ubiquitous, diverse, from space. However, during nonbloom trophic—they ingest prey—usually other and major participants in oceanic food seasons, even smaller cells (picoplank- microbes. Some heterotrophic protists webs and in marine biogeochemical ton— and less are parasites of (Kuhn et cycles. The study and characterization than a few micrometers in size) typi- al., 2004) or (Théodorides, of protists has a long and distinguished cally dominate phytoplankton 1987), while still others form symbiotic tradition. Even with this history, the and production (Li, 2002; Worden et al., relationships with autotrophic or het- erotrophic (Foster et al., 2006; Guillou et al., 1999). In addition, many ...the extraordinary and species of protists have mixed trophic modes. These “” include variety of interactions of protists in the flagellated phytoplankton that ingest sea are only now being fully appreciated. bacteria or other protists (Caron, 2000), that “farm” from ingested algal prey (Stoecker, 1992), and ll rights reserved. Permission is reserved. ll rights granted to in teaching copy this and research. for use article R extraordinary species diversity and vari- 2004). Some genera of marine picoal- mutualistic relationships between pho- ety of interactions of protists in the sea gae can “bloom” to very high concen- tosynthetic and hetero- are only now being fully appreciated. trations (> 105 cells ml-1), trophic protists (Caron and Swanberg, Figure 1 shows representative examples (Countway and Caron, 2006), while oth- 1990). Heterotrophic nutrition occurs of , and of methods used ers are ubiquitous, such as , among virtually all lineages of protists. to visualize these microbes. which is found from arctic to tropical Some protistan groups formerly clas- Protists can be autotrophic or het- waters (Not et al., 2004; Worden, 2006). sified as “” include species with erotrophic. The former, also called In contrast to photosynthetic pro- strictly heterotrophic nutrition. For microscopic algae, contain chloroplasts, tists, heterotrophic protists have no per- example, the include thrive by , and are at the manent chloroplasts and rely on other many heterotrophic species (Lessard, base of all oceanic food webs, with the exception of deep-sea chemosynthetic Barry F. Sherr ([email protected]) is Professor, College of Oceanic and . There is a general trend for Atmospheric Sciences, Oregon State University, Corvallis, OR, USA. Evelyn B. Sherr is > 20-µm sized phytoplankton (micro- Professor, College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, ), such as and dino- OR, USA. David A. Caron is Professor, Department of Biological Sciences, University of ockville, M D 20849-1931, U ockville, , to dominate episodically in Southern California, Los Angeles, CA, USA. Daniel Vaulot is Directeur de Recherche at epublication, systemmatic reproduction, coastal waters, while in the open the Station Biologique de Roscoff, UMR 7144 CNRS and Université Pierre et Marie Curie, 2–20-µm sized cells (nanoplankton), France. Alexandra Z. Worden is Assistant Professor, Rosenstiel School of Marine and such as coccolithophorids, sporadically Atmospheric Science, University of Miami, Miami, FL, USA. S A .

130 Oceanography Vol. 20, No. 2 1991; Jeong, 1999), and it is possible that all dinoflagellates, including the photosynthetic species responsible for red tides, may have the capacity for phagotrophy (H.J. Jeong, Seoul National University, pers. comm., July 2006). Phagotrophic protists have long been known to be important in oce- anic food webs as consumers of bacteria and phytoplankton (reviewed in Strom, 2000; Sherr and Sherr, 2002; Calbet and Landry, 2004), as regenerators of nutri- ents for further phytoplankton growth (Caron and Goldman, 1990), and as a food for marine zooplankton (Stoecker and Capuzzo, 1990). The graz- ing impact of phagotrophic protists has consequences for both mod- eling and for the structure of microbial communities. The proportion of organic carbon produced by phytoplankton that flows through a multi-step micro- bial versus a shorter phyto- plankton-mesozooplankton is a critical factor that determines the capacity of marine ecosystems to seques- ter organic carbon and to efficiently Figure 1. Examples of marine protists and of methods used to visualize eukaryotic microbes: produce fish biomass (Legendre and (A) Live cells of the 2-µm-diameter marine flagellated algaPelagomonas calceolate, trans- Le Fevre, 1995). Via selective grazing, mitted light microscopy. (B) Two cells of a 5-µm-long marine heterotrophic Bodo( sp.), scanning electron microscopy (SEM). (C) A 50-µm-diameter autotrophic thecate dino- both herbivorous and bacterivorous pro- flagellate Lingulodinium( polyedrum) that forms blooms, SEM. (D) Two cells of a tists can alter the composi- 20 x 60 µm marine heterotrophic Gyrodinium( sp.) with food full of ingested coccoid , epifluorescence microscopy after preservation with form- tion of oceanic phytoplankton (Strom aldehyde and with the fluorochrome AD PI. (E) The 55-µm-diameter marine pelagic and Loukos, 1998) and bacterial assem- Strombilidium sp., inverted light microscopy after preservation with acid Lugol fixative. blages (Suzuki, 1999; Jurgens and Matz, (F) Live foraminiferan Hastigerina pelagica with a fluid bubble capsule and a approxi- mately 300 µm across, darkfield light microscopy.Sources of micrographs: (A) culture collec- 2002). It is clear that these activities tion of the Station Biologique Roscoff (planktonnet.sb-roscoff.fr); (B) laboratory of John Sieburth, constitute major roles in oceanic eco- courtesy of Dave Caron; (D) and (E) B. and E. Sherr; (C) and (F) Dave Caron systems, and considerable information has been amassed on the abundances, distributions, and ecological roles of protists, yet there is still much to learn. At present, much of our knowledge is restricted to larger species that have readily identifiable morphological traits

Oceanography June 2007 131 and those species that are amenable to late (Groisillier et al., 2006) and stra- graphically restricted gene flow) among laboratory culture. menopile (Massana et al., 2006) divisions species of ciliates in isolated tide pools. One fundamental question that has have escaped detection until recently. Little is known at this juncture about become a focus of research and debate The discovery of many cryptic lineages the distribution, gene flow, diversity, in recent years revolves around the spe- highlights the importance of combining ecological roles, or even the morpholo- cies concept (and species boundaries) for molecular and ecological information gies of the previously undescribed lin- protists. Although protistan species have with traditional morphological descrip- eages of protists now being revealed by traditionally been defined based on their tions. This combination facilitates mean- molecular analyses. morphology, recent molecular analy- ingful investigation of the distribution Beyond characterizing the diversity ses and physiological studies reveal that and activities of marine protists in situ and distribution of protists in the ocean, even well-defined morphospecies may (Modeo et al., 2003). major lines of research continue to elu- be composed of a mosaic of multiple These new approaches for defin- cidate the ecological roles of protists genetic/physiological types. For instance, ing protistan species have energized an in marine ecosystems. Species-specific the ubiquitous Skeletonema ongoing debate regarding protistan spe- growth, grazing, and nutrient excre- costatum, thought until recently to be cies diversity and . The tion rates of heterotrophic protists are a single species, is actually a composite overarching question is whether there derived mainly from laboratory experi- of ten genetic types that are now con- are relatively few species of protists that ments using isolated species fed mono- sidered distinct species (Zingone et al., are broadly distributed, or whether simi- specific prey under conditions that 2005; Sarno et al., 2005). Similarly, physi- lar protistan morphotypes are in fact poorly mimic natural systems. However, ological variability among Spumella- distinct species or subspecies with more such studies show that phagotrophic like heterotrophic flagellates indicates limited distribution (Fenchel, 2005; Katz protists exhibit various types of spe- geographically distinct adaptations and et al., 2005). Why does species diversity cies-specific behavior that may affect emphasizes that morphology needs to be matter? From an ecological perspective, feeding behavior and growth, including complemented by other approaches for it is important to know what taxonomic chemosensory responses to prey and distinguishing different species (Boenigk level (e.g., species or subspecies) yields selective ingestion of prey types (Strom, et al., 2006). The situation is even more information about associated differ- 2000; Wolfe, 2000). In turn, prey cells may use structural or chemical defenses against protistan (Wolfe, 2000; Jurgens and Matz, 2002; Matz et al., ...many fascinating discoveries are ahead for 2004). Research on the underlying physi- protistan researchers at the physiological, ological/biochemical basis of the feeding behavior of marine protists is yielding organismal, and community levels. new awareness and understanding of their predator-prey interactions (Wolfe, 2000; Wooten et al., 2006). The ability complicated for the tiny picoplanktonic ences in functional roles (i.e., how these of herbivorous protists to discriminate protists in the ocean. Molecular analyses organisms participate in food webs). between alternate prey types depending during the last ten years have revealed Based on analysis of genetic variation, on size and “taste” (Verity, 1991; Hansen, many undescribed and uncultivated taxa Katz et al. (2005) found evidence for a 1992; Strom et al., 2003; Wooten et al., among these morphologically similar “cosmopolitan” distribution (high gene 2006) undoubtedly affects protistan forms (Moon-van der Staay et al., 2001; flow and low diversity) for species of grazing impact on bloom-forming phy- López-García et al., 2001; Diéz et al., ciliates in coastal waters and evidence toplankton, such as diatoms and harm- 2001), and whole lineages in the alveo- for “endemism” (high diversity and geo- ful algal species (Jeong, 1999). Studies

132 Oceanography Vol. 20, No. 2 of protistan herbivory on in situ phy- ing oceanic plankton community struc- of planktonic sarcodines. Reviews in Aquatic Sciences 3:147–180. toplankton communities indicate that ture and production; both are known to Countway, P.D., and D.A. Caron. 2006. food quality can play an important role occur (Foster, 2006), but little is known and distribution of Ostreococcus sp. in the in grazer selectivity (e.g., Worden and about their prevalence and extent in San Pedro Channel, California, as revealed by quantitative PCR. Applied and Environmental Binder, 2003) and that protistan growth marine systems. 72:2,496–2,506. efficiencies vary greatly with prey type Breakthroughs will depend on Courties, C., A. Vaquer, M. Troussellier, J. Lautier, (e.g., Guillou et al., 2001). Accurately the application of a diverse array of M.J. Chrétiennot-Dinet, J. Neveux, C. Machado, and H. Claustre. 1994. Smallest eukaryotic describing the rates of activity of hetero- approaches and methodologies. These organism. Nature 370:255. trophic protists is extremely important will almost assuredly hold implications Derelle, E., C. Ferraz, S. Rombauts, P. Rouzé, to carbon-cycle models. even beyond the important roles these A.Z. Worden, S. Robbens, F. Partensky, S. Degroeve, S. Echeynié, R. Cooke, and others. Unquestionably, many fascinating dis- organisms are already known to play 2006. analysis of the smallest free-liv- coveries are ahead for protistan research- in oceanic ecosystems. Marine protists ing Ostreococcus tauri unveils many ers at the physiological, organismal, and likely retain some characteristics of unique features. Proceedings of the National Academy of Sciences of the United States of community levels. These include: the earliest eukaryotes that evolved on America 103:11,647–11,652. • characterizing the overall breadth and Earth. Interrogation of their Diéz, B., C. Pedrós-Alió, and R. Massana. 2001. meaning of protistan species diversity provides insights into how they thrive in Study of genetic diversity of eukaryotic pico- plankton in different oceanic regions by in the ocean; the world’s ocean (Ambrust et al., 2005; small-subunit rRNA gene cloning and sequenc- • understanding the of min- Derelle et al., 2006) and insights into ing. Applied and Environmental Microbiology 67:2,932–2,941. ute organisms, such as the 2 µm het- fundamental biological processes such as Fenchel, T. 2005. Cosmopolitan microbes and erotrophic flagellate Symbiomonas the evolution of multicellularity (King their ‘cryptic’ species. Aquatic scintillans that itself harbors an endo- et al., 2004), and thus will foster a better 41:49–54. Foster, R.A., J.L. Collier, and E.J. Carpenter. 2006. symbiotic bacterium (Guillou et al., understanding of the evolution of life on Reverse transcription PCR amplification of cya- 1999) and the pico-alga Ostreococcus our planet. nobacterial symbiont 16s rRNA sequences from tauri, the smallest free-living eukary- single non-photosynthetic eukaryotic marine planktonic host cells. Journal of Phycology ote known (Courties et al., 1994), References 42:243–250 which can occur at high abun- Armbrust, E.V., J.A. Berges, C. Bowler, B.R. Gast, R.J., D.M. Moran, M.R. Dennett, and D.A. Green, Diego Martinez, Nicholas H. Putnam, dances (Countway and Caron, 2006) Caron. 2007. in an Antarctic dino- Shiguo Zhou, Andrew E. Allen, and others. flagellate: caught in evolutionary transition? and has unique genome features 2004. The genome of the diatom Thalassiosira Environmental Microbiology 9(1):39–45, doi: (Derelle et al., 2006); pseudonana: Ecology, evolution, and metabo- 10.1111/j.1462-2920.2006.01109.x. lism. Science 306:79-86. • deciphering the ecological, molecular, Groisillier, A., R. Massana, K. Valentin, D. Vaulot, Boenigk, J., K. Pfandl, T. Garstecki, H. Harms, G. and L. Guillou. 2006. Genetic diversity and hab- and biochemical processes that might Novarino, and A. Chatzinotas. 2006. Evidence itats of two enigmatic marine lineages. explain acquisition by for geographic isolation and signs of endemism Aquatic Microbial Ecology 42:277–291. within a protistan morphospecies. Applied and Guillou, L., M. Chrétiennot-Dinet, S. Boulben, heterotrophic protists (Gast et al., in Environmental Microbiology 72:5,159–5,164. S. Moon-van der Staay, and D. Vaulot. 1999. press); and Calbet, A., and M.R. Landry. 2004. Phytoplankton Symbiomonas scintillans gen. et sp nov • characterizing microbial interactions growth, microzooplankton grazing, and car- and Picophagus flagellatusgen. et sp nov bon cycling in marine systems. and (Heterokonta): Two new heterotrophic flagel- and processes sufficiently to provide Oceanography 40:51–57. lates of picoplanktonic size. 150:383–398. a predictive understanding of com- Caron, D.A. 2000. and mixotrophy Guillou, L., S. Jacquet, M. Chrétiennot-Dinet, and munity function and how microbial among pelagic microorganisms. Pp. 495–523 in D. Vaulot. 2001. Grazing impact of two small Microbial Ecology of the . D.L. Kirchman, heterotrophic flagellates on Prochlorococcus communities will respond in the face ed., Wiley-Liss, New York. and Synechococcus. Aquatic Microbial Ecology of environmental change. Caron, D.A., and J.C. Goldman. 1990. Nutrient 26:201–207. Yet another challenge ahead is to under- regeneration. Pp. 283– 306 in Ecology of Marine Hansen, P.J. 1992. size selection, feeding . G.M. Capriulo, ed., Oxford University rates and growth dynamics of marine hetero- stand the importance of processes such Press, New York. trophic dinoflagellates, with special empha- as and symbiosis in regulat- Caron, D.A., and N.R. Swanberg. 1990. The ecology sis on Gyrodinium spirale.

Oceanography June 2007 133 114:327–334. from reveal unsuspected eukary- Worden, A.Z. 2006. diversity in Jeong, H.J. 1999. The ecological roles of hetero- otic diversity. Nature 409:607–610. coastal waters of the Pacific Ocean. Aquatic trophic dinoflagellates in marine planktonic Not, F., R. Massana, M. Latasa, D. Marie, C. Colson, Microbial Ecology 43:165–175. community. Journal of Eukaryotic Microbiology W. Eikrem, C. Pedros-Alio, D. Vaulot, and M. Worden, A.Z., and B.J. Binder. 2003. Application 46:390–396. Simon. 2005. Late summer community com- of dilution experiments for measuring growth Jurgens, K., and C. Matz. 2002. Predation as a shap- position and abundance of photosynthetic and mortality rates among Prochlorococcus ing force for the phenotypic and genotypic in Norwegian and Barents Seas. and Synechococcus populations in oligotro- composition of planktonic bacteria. Antonie Limnology and Oceanography 50:1,677–1,686. phic environments. Aquatic Microbial Ecology Van Leewenhoek International Journal of General Sarno, D., W.H.C.F. Kooistra, L. Medlin, I. Percopo, 30:159–174. and Molecular Microbiology 81:413–434. and A. Zingone. 2005. Diversity in the genus Worden A.Z., J.K. Nolan, and B. Palenik 2004. Katz, L.A,, G.B. McManus, O.L.O. Snoeyenbos- Skeletonema (Bacillariophyceae). II. An assess- Assessing the dynamics and ecology of West, A. Griffin, K. Pirog, B. Costas, and W. ment of the taxonomy of S. costatum-like spe- marine picophytoplankton: The importance Foissner. 2005. Reframing the ‘Everything is cies with the description of four new species. of the eukaryotic component. Limnology and everywhere’ debate: Evidence for high gene flow Journal of Phycology 41:151–176. Oceanography 49:168–179. and diversity in ciliate morphospecies. Aquatic Sherr, E.B., and B.F. Sherr. 2002. Significance of Zingone, A., I. Percopo, P.A. Sims, and D. Sarno. Microbial Ecology 41:55–65. predation by protists in aquatic microbial food 2005. Diversity in the genus Skeletonema King, N. 2004. The unicellular ancestry of webs. Antonie Van Leewenhoek International (Bacillariophyceae): I. A reexamination of the development. Developmental Cell 7:313–325. Journal of General and Molecular Microbiology type material of S. costatum with the descrip- Kuhn, S., L. Medlin, and G. Eller. 2004. 81:293–308. tion of S. grevillei sp. nov. Journal of Phycology Phylogenetic position of the parasitoid nano- Stoecker, D.K. 1992. “” that photosynthe- 41:140–50. flagellate Pirsonia inferred from nuclear- size and “” that eat. Oceanus 35:24–27. encoded small subunit ribosomal DNA and Stoecker, D.K., and J.M. Capuzzo. 1990. Predation a description of Pseudopirsonia n. gen. and on protozoa: Its importance to zooplankton. Pseudopirsonia mucosa (Drebes) comb. nov. Journal of Plankton Research 12:891–908. Protist 155:143–156. Strom, S.L. 2000. Bacterivory: Interactions Legendre, L., and J. Le Fevre. 1995. Microbial food between bacteria and their grazers. Pp 351–286 webs and the export of biogenic carbon in in Microbial Ecology of the Oceans. D.L. oceans. Aquatic Microbial Ecology 9:69–77. Kirchman, ed., Wiley-Liss, New York. Lessard, E.J. 1991. The trophic role of heterotrophic Strom, S.L., and H. Loukos. 1998. Selective feeding dinoflagellates in diverse marine environments. by protozoa: Model and experimental behaviors Marine Microbial Food Webs 5:49–58. and their consequences for population stability. Li, W.K.W. 2002. Macroecological patterns of phy- Journal of Plankton Research 20:831–846. toplankton in the northwestern North Atlantic Strom, S. L., G.V. Wolfe, J.L. Holmes, H.A. Stecher, Ocean. Nature 419:154–157. C. Shimeneck, S. Lambert, and E. Moreno. López-Garcia, P., F. Rodríguez-Valera, C. Pedrós- 2003. Chemical defense in the microplankton: Alió, and D. Moreira. 2001. Unexpected diver- I. Feeding and growth rates of heterotrophic sity of small eukaryotes in deep-sea Antarctic protists on the DMS-producing phytoplankter plankton. Nature 409:603–607. . Limnology and Oceanography Massana, R., R. Terrado, I. Forn, C. Lovejoy, and 48:217–229. C. Pedrós-Alió. 2006. Distribution and abun- Suzuki, M.T. 1999. Effect of protistan bacterivory dance of uncultured heterotrophic flagellates in on coastal diversity. Aquatic the world oceans. Environmental Microbiology Microbial Ecology 20:261–272. 8:1,515–1,522. Théodorides, J. 1987. Parasitology of marine Matz, C., P. Deines, J. Boenigk, H. Arndt, L. Eberl, zooplankton. Advances in Marine Biology S. Kjelleberg, and K. Jurgens. 2004. Impact 25:117–177. of violacein-producing bacteria on survival Verity, P.G. 1991. Feeding in planktonic protozoans: and feeding of bacterivorous nanoflagel- Evidence for non-random acquisition of prey. lates. Applied and Environmental Microbiology Marine Microbial Food Webs 5:69–76. 70:1,593–1,599. Wolfe, G.V. 2000. The chemical defense ecology Modeo, L., G. Petroni, G. Rosati, and D.J.S. of marine unicellular plankton: Constraints, Montagnes. 2003. A multidisciplinary mechanisms, and impacts. The Biological approach to describe protists: Redescriptions of Bulletin 198:225–244. Novistrombidium testaceum Anigstein 1914 and Wootton, E.C., M.V. Zubkov, D.H. Jones, R.H. Strombidium inclinatum Montagnes, Taylor and Jones, C.M. Martel, C.A. Thornton, and E.C. Lynn 1990 (Ciliophora, Oligotrichia). Journal of Roberts. 2006. Biochemical prey recogni- Eukaryotic Microbiology 50(3):175–189. tion by planktonic protozoa. Environmental Moon-Van Der Staay, S.Y., R. De Wachter, and D. Microbiology doi:10.1111/j.1462- Vaulot. 2001. Oceanic 18S rDNA sequences 2920.2006.01130.x.

134 Oceanography Vol. 20, No. 2