全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...

Biology of the Marine Heterotrophic Dinoflagellate Oxyrrhis marina: Current Status and Future Directions

DOI: 10.3390/microorganisms1010033

Keywords: heterotrophic dinoflagellates, protist, Oxyrrhis marina, biology

Full-Text   Cite this paper   Add to My Lib

Abstract:

Heterotrophic dinoflagellates are prevalent protists in marine environments, which play an important role in the carbon cycling and energy flow in the marine planktonic community. Oxyrrhis marina (Dinophyceae), a widespread heterotrophic dinoflagellate, is a model species used for a broad range of ecological, biogeographic, and evolutionary studies. Despite the increasing research effort on this species, there lacks a synthesis of the existing data and a coherent picture of this organism. Here we reviewed the literature to provide an overview of what is known regarding the biology of O. marina, and identify areas where further studies are needed. As an early branch of the dinoflagellate lineage, O. marina shares similarity with typical dinoflagellates in permanent condensed chromosomes, less abundant nucleosome proteins compared to other eukaryotes, multiple gene copies, the occurrence of trans-splicing in nucleus-encoded mRNAs, highly fragmented mitochondrial genome, and disuse of ATG as a start codon for mitochondrial genes. On the other hand, O. marina also exhibits some distinct cytological features (e.g., different flagellar structure, absence of girdle and sulcus or pustules, use of intranuclear spindle in mitosis, presence of nuclear plaque, and absence of birefringent periodic banded chromosomal structure) and genetic features (e.g., a single histone-like DNA-associated protein, cob- cox3 gene fusion, 5′ oligo-U cap in the mitochondrial transcripts of protein-coding genes, the absence of mRNA editing, the presence of stop codon in the fused cob- cox3 mRNA produced by post-transcriptional oligoadenylation, and vestigial plastid genes). The best-studied biology of this dinoflagellate is probably the prey and predators types, which include a wide range of organisms. On the other hand, the abundance of this species in the natural waters and its controlling factors, genome organization and gene expression regulation that underlie the unusual cytological and ecological characteristics are among the areas that urgently need study.

References

[1]  Sherr, E.B.; Sherr, B.F. Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 2002, 81, 293–308, doi:10.1023/A:1020591307260.
[2]  Roberts, E.C.; Wootton, E.C.; Davidson, K.; Jeong, H.J.; Lowe, C.D.; Montagnes, D.J.S. Feeding in the dinoflagellate Oxyrrhis marina: Linking behaviour with mechanisms. J. Plankton Res. 2011, 33, 603–614, doi:10.1093/plankt/fbq118.
[3]  Yang, Z.; Jeong, H.J.; Montagnes, D.J.S. The role of Oxyrrhis marina as a model prey: Current work and future directions. J. Plankton Res. 2011, 33, 665–675, doi:10.1093/plankt/fbq112.
[4]  Lowe, C.D.; Martin, L.E.; Montagnes, D.J.; Watts, P.C. A legacy of contrasting spatial genetic structure on either side of the Atlantic–Mediterranean transition zone in a marine protist. Proc. Natl. Acad. Sci. USA 2012, 109, 20998–21003, doi:10.1073/pnas.1214398110.
[5]  Jeong, H.J. The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryot. Microbiol. 1999, 46, 190–396.
[6]  Sherr, E.B.; Sherr, B.F. Heterotrophic dinoflagellates: A significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar. Ecol. Prog. Ser. 2007, 352, 187–197, doi:10.3354/meps07161.
[7]  Hansen, P.J. Dinophysis—A planktonic dinoflagellate genus which can act both as a prey and a predator of a ciliate. Mar. Ecol. Prog. Ser. 1991, 69, 201–204, doi:10.3354/meps069201.
[8]  Jeong, H.J.; Seong, K.A.; Yoo, Y.D.; Kim, T.H.; Kang, N.S.; Kim, S.; Park, J.Y.; Kim, J.S.; Kim, G.H.; Song, J.Y. Feeding and grazing impact by small marine heterotrophic dinoflagellates on heterotrophic bacteria. J. Eukaryot. Microbiol. 2008, 55, 271–288, doi:10.1111/j.1550-7408.2008.00336.x.
[9]  Slamovits, C.H.; Keeling, P.J. Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Mol. Biol. Evol. 2008, 25, 1297–1306, doi:10.1093/molbev/msn075.
[10]  Lowe, C.D.; Keeling, P.J.; Martin, L.E.; Slamovits, C.H.; Watts, P.C.; Montagnes, D.J.S. Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. J. Plankton Res. 2011, 33, 555–567, doi:10.1093/plankt/fbq110.
[11]  Watts, P.C.; Martin, L.E.; Kimmance, S.A.; Montagnes, D.J.; Lowe, C.D. The distribution of Oxyrrhis marina: A global disperser or poorly characterized endemic? J. Plankton Res. 2011, 33, 579–589, doi:10.1093/plankt/fbq148.
[12]  Tillmann, U. Phagotrophy by a plastidic haptophyte, Prymnesium patelliferurn. Aquat. Microb. Ecol. 1998, 14, 155–160, doi:10.3354/ame014155.
[13]  Tillmann, U. Kill and eat your predator: A winning strategy of the planktonic flagellate Prymnesium parvum. Aquat. Microb. Ecol. 2003, 32, 73–84, doi:10.3354/ame032073.
[14]  Suttle, C.A. Marine viruses-major players in the global ecosystem. Nat. Rev. Microbiol. 2007, 5, 801–812, doi:10.1038/nrmicro1750.
[15]  Mariani, P.; Botte, V.; Ribera d’Alcalà, M. A numerical investigation of the impact of turbulence on the feeding rates of Oithona davisae. J. Mar. Syst. 2008, 70, 273–286, doi:10.1016/j.jmarsys.2006.04.020.
[16]  Boakes, D.E.; Codling, E.A.; Thorn, G.J.; Steinke, M. Analysis and modelling of swimming behaviour in Oxyrrhis marina. J. Plankton Res. 2011, 33, 641–649, doi:10.1093/plankt/fbq136.
[17]  Lowe, C.D.; Day, A.; Kemp, S.J.; Montagnes, D.J. There are high levels of functional and genetic diversity in Oxyrrhis marina. J. Eukaryot. Microbiol. 2005, 52, 250–257, doi:10.1111/j.1550-7408.2005.00034.x.
[18]  Montagnes, D.J.S.; Lowe, C.D.; Martin, L.; Watts, P.C.; Downes-Tettmar, N.; Yang, Z.; Roberts, E.C.; Davidson, K. Oxyrrhis marina growth, sex and reproduction. J. Plankton Res. 2011, 33, 615–627, doi:10.1093/plankt/fbq111.
[19]  Hartz, A.J.; Sherr, B.F.; Sherr, E.B. Photoresponse in the heterotrophic marine dinoflagellate Oxyrrhis marina. J. Eukaryot. Microbiol. 2011, 58, 171–177, doi:10.1111/j.1550-7408.2011.00529.x.
[20]  Montagnes, D.J.S.; Lowe, C.D.; Roberts, E.C.; Breckels, M.N.; Boakes, D.E.; Davidson, K.; Keeling, P.J.; Slamovits, C.H.; Steinke, M.; Yang, Z.; et al. An introduction to the special issue: Oxyrrhis marina, a model organism? J. Plankton Res. 2011, 33, 549–554, doi:10.1093/plankt/fbq121.
[21]  Van Meel, L. Etudes hydrobiologiques des eaux saumatres de belgique: 3. Les étangs galgenweelen à anvers (rive gauche). Bull. K. Belg. Inst. Nat. Wet. 1958, 34, 1–20. (in French).
[22]  Scheffel, A. Phaeocystis globosa nov. Spec. Nebst einigen betrachtungen über die phylogenie niederer, insbesondere brauner organismen. In Wissenschaftliche Meeresuntersuchungen. (in German); Abteilung Helgoland N. F.: Helgoland, Germany, 1900; Volume 4, pp. 1–29.
[23]  Conrad, W. Notes protistologiques ix surtroisdinoflagellates de l’eausaumatre. Bull. Mus. Roy. Hist. Nat. Belg. 1939, 15, 1–10. (in French).
[24]  Kofoid, C.A.; Swezy, O. The Free-Living Unarmored Dinoflagellata; University of California Press: Berkeley, CA, USA, 1921; Volume 5, p. 538.
[25]  Dodge, J.D.; Hart-Jones, B. Marine Dinoflagellates of the British Isles; HMSO: London, UK, 1982.
[26]  Cavalier-Smith, T.; Chao, E. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. Nov.). Eur. J. Protistol. 2004, 40, 185–212, doi:10.1016/j.ejop.2004.01.002.
[27]  Lowe, C.D.; Montagnes, D.J.S.; Martin, L.E.; Watts, P.C. Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (alveolata: Dinophyceae). Protist 2010, 161, 212–221, doi:10.1016/j.protis.2009.11.003.
[28]  Lowe, C.D.; Montagnes, D.J.; Martin, L.E.; Watts, P.C. High genetic diversity and fine-scale spatial structure in the marine flagellate Oxyrrhis marina (Dinophyceae) uncovered by microsatellite loci. PLoS One 2010, 5, e15557.
[29]  Lowe, C.D.; Martin, L.E.; Roberts, E.C.; Watts, P.C.; Wootton, E.C.; Montagnes, D.J.S. Collection, isolation, and culturing strategies for Oxyrrhis marina. J. Plankton Res. 2011, 33, 569–578, doi:10.1093/plankt/fbq161.
[30]  Cachon, J.; Cachon, M.; Salvano, P. The nuclear division of Oxyrrhis marina: An example of the role played by the nuclear envelope in chromosome segregation. Arch. Protistenk. 1979, 122, 43–54, doi:10.1016/S0003-9365(79)80019-6.
[31]  Kato, K.H.; Moriyama, A.; Itoh, T.J.; Yamamoto, M.; Horio, T.; Huitorel, P. Dynamic changes in microtubule organization during division of the primitive dinoflagellate Oxyrrhis marina. Biol. Cell 2000, 92, 583–594, doi:10.1016/S0248-4900(00)01106-0.
[32]  Saldarriaga, J.F. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int. J. Syst. Evol. Microbiol. 2003, 53, 355–365, doi:10.1099/ijs.0.02328-0.
[33]  Lenaers, G.; Scholin, C.; Bhaud, Y.; Saint-Hilaire, D.; Herzog, M. A molecular phylogeny of dinoflagellate protists (pyrrhophyta) inferred from the sequence of 24S rRNA divergent domains d1 and d8. J. Mol. Evol. 1991, 32, 53–63, doi:10.1007/BF02099929.
[34]  Slamovits, C.H.; Saldarriaga, J.F.; Larocque, A.; Keeling, P.J. The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both apicomplexan and dinoflagellate mitochondrial genomes. J. Mol. Biol. 2007, 372, 356–368, doi:10.1016/j.jmb.2007.06.085.
[35]  Leander, B.S.; Keeling, P.J. Early evolutionary history of dinoflagellates and apicomplexans (alveolata) as inferred from HSP90 and actin phylogenies. J. Phycol. 2004, 40, 341–350, doi:10.1111/j.1529-8817.2004.03129.x.
[36]  Zhang, H.; Lin, S. mRNA editing and spliced-leader RNA trans-splicing groups Oxyrrhis, Noctiluca, Heterocapsa, and Amphidiniumas basal lineages of dinoflagellates. J. Phycol. 2008, 44, 703–711, doi:10.1111/j.1529-8817.2008.00521.x.
[37]  Clarke, K.; Pennick, N. The occurrence of body scales in Oxyrrhis marina dujardin. Br. Phycol. J. 1976, 11, 345–348, doi:10.1080/00071617600650391.
[38]  Clarke, K.; Pennick, N. Flagellar scales in Oxyrrhis marina dujardin. Br. Phycol. J. 1972, 7, 357–360, doi:10.1080/00071617200650371.
[39]  Cachon, M.; Cosson, J.; Cosson, M.P.; Huitorel, P.; Cachon, J. Ultrastructure of the flagellar apparatus of Oxyrrhis marina. Biol. Cell 1988, 63, 159–168, doi:10.1016/0248-4900(88)90055-X.
[40]  Roberts, K.R. The flagellar apparatus of Oxyrrhis marina (pyrrophyta). J. Phycol. 1985, 21, 641–655, doi:10.1111/j.0022-3646.1985.00641.x.
[41]  Roberts, K.; Roberts, J.E. The Flagellar Apparatus and Cytoskeleton of the Dinoflagellates. Protoplasma 1991, 164, 105–122, doi:10.1007/BF01320818.
[42]  Kato, K.H.; Moriyama, A.; Huitorel, P.; Cosson, J.; Cachon, M.; Sato, H. Isolation of the major basic nuclear protein and its localization on chromosomes of the dinoflagellate Oxyrrhis marina. Biol. Cell 1997, 89, 43–52, doi:10.1016/S0248-4900(99)80080-X.
[43]  Zhang, H.; Hou, Y.; Miranda, L.; Campbell, D.A.; Sturm, N.R.; Gaasterland, T.; Lin, S. Spliced leader RNA trans-splicing in dinoflagellates. Proc. Natl. Acad. Sci. USA 2007, 104, 4618–4623.
[44]  Zhang, H.; Zhuang, Y.; Gill, J.; Lin, S. Proof that dinoflagellate spliced leader (dinosl) is a useful hook for fishing dinoflagellate transcripts from mixed microbial samples: Symbiodinium kawagutii as a case study. Protist 2013, 164, 510–527, doi:10.1016/j.protis.2013.04.002.
[45]  Hall, R.P. Binary Fission in Oxyrrhis marina Dujardin. University of California Press: Berkeley, CA, USA, 1925; Volume 26, pp. 281–324.
[46]  Triemer, R.E. A unique mitotici variation in the marine dinoflagellate Oxyrrhis marina (pyrrophyta). J. Phycol. 1982, 18, 399–411, doi:10.1111/j.1529-8817.1982.tb03202.x.
[47]  Gao, X.; Li, J. Nuclear division in the marine dinoflagellate Oxyrrhis marina. J. Cell Sci. 1986, 85, 161–175.
[48]  Sano, J.; Kato, K.H. Localization and copy number of the protein-codinggenes actin, α-tubulin, and HSP90 in the nucleus of a primitive dinoflagellate, Oxyrrhis marina. Zool. Sci. 2009, 26, 745–753, doi:10.2108/zsj.26.745.
[49]  Slamovits, C.H.; Keeling, P.J. Contributions of Oxyrrhis marina to molecular biology, genomics and organelle evolution of dinoflagellates. J. Plankton Res. 2011, 33, 591–602, doi:10.1093/plankt/fbq153.
[50]  Coats, D.W. Dinoflagellate life-cycle complexities. J. Phycol. 2002, 38, 417–419, doi:10.1046/j.1529-8817.2002.03832.x.
[51]  Santos, S.R.; Coffroth, M.A. Molecular genetic evidence that dinoflagellates belonging to the genus Symbiodinium freudenthal are haploid. Biol. Bull. 2003, 204, 10–20.
[52]  Hausmann, K.; Hülsmann, N.; Radek, R. Protistology; E. Schweizerbart’sche Verlagsbuchhandlung: Berlin, Germany, 2003.
[53]  Hackett, J.D.; Anderson, D.M.; Erdner, D.L.; Bhattacharya, D. Dinoflagellates: A remarkable evolutionary experiment. Am. J. Bot. 2004, 91, 1523–1534, doi:10.3732/ajb.91.10.1523.
[54]  Veldhuis, M.J.W.; Cucci, T.L.; Sieracki, M.E. Cellular DNA content of marine phytoplankton using two new fluorochromes: Taxonomic and ecological implications. J. Phycol. 1997, 33, 527–541.
[55]  LaJeunesse, T.C.; Lambert, G.; Anderson, R.A.; Coffroth, M.A.; Galbraith, D.W. Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J. Phycol. 2005, 41, 880–886.
[56]  Le, Q.; Markovic, P.; Hastings, J.; Jovine, R.; Morse, D. Structure and organization of the peridinin-chlorophyll a-binding protein gene in Gonyaulax polyedra. Mol. Gen. Genet. 1997, 255, 595–604.
[57]  Reichman, J.R.; Wilcox, T.P.; Vize, P.D. PCP gene family in Symbiodinium from Hippopus hippopus: Low levels of concerted evolution, isoform diversity, and spectral tuning of chromophores. Mol. Biol. Evol. 2003, 20, 2143–2154.
[58]  Bachvaroff, T.R.; Place, A.R. From stop to start: Tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 2008, 3, e2929, doi:10.1371/journal.pone.0002929.
[59]  Galluzzi, L.; Bertozzini, E.; Penna, A.; Perini, F.; Garcés, E.; Magnani, M. Analysis of rRNA gene content in the mediterranean dinoflagellate Alexandrium catenella and Alexandrium taylori: Implications for the quantitative real-time PCR-based monitoring methods. J. Appl. Phycol. 2009, 22, 1–9.
[60]  Erdner, D.L.; Percy, L.; Keafer, B.; Lewis, J.; Anderson, D.M. A quantitative real-time PCR assay for the identification and enumeration of Alexandrium cysts in marine sediments. Deep Sea Res. Part II Top. Stud. Oceanogr. 2010, 57, 279–287, doi:10.1016/j.dsr2.2009.09.006.
[61]  Zhang, H.; Lin, S. Complex gene structure of the form II Rubisco in the dinoflagellate Prorocentrum minimum (Dinophyceae). J. Phycol. 2003, 39, 1160–1171, doi:10.1111/j.0022-3646.2003.03-055.x.
[62]  Li, L.; Hastings, J.W. The structure and organization of the luciferase gene in the photosynthetic dinoflagellate Gonyaulax polyedra. Plant Mol. Biol. 1998, 36, 275–284.
[63]  Zhang, H.; Hou, Y.; Lin, S. Isolation and characterization of proliferating cell nuclear antigen from the dinoflagellate Pfiesteria piscicida. J. Eukaryot. Microbiol. 2006, 53, 142–150, doi:10.1111/j.1550-7408.2005.00085.x.
[64]  Zhang, H.; Dungan, C.F.; Lin, S. Introns, alternative splicing, spliced leader trans-splicing and differential expression of pcna and cyclin in Perkinsus marinus. Protist 2011, 162, 154–167.
[65]  Beauchemin, M.; Roy, S.; Daoust, P.; Dagenais-Bellefeuille, S.; Bertomeu, T.; Letourneau, L.; Lang, B.F.; Morse, D. Dinoflagellate tandem array gene transcripts are highly conserved and not polycistronic. Proc. Natl. Acad. Sci. USA 2012, 109, 15793–15798.
[66]  Lowe, C.D.; Mello, L.V.; Samatar, N.; Martin, L.E.; Montagnes, D.J.S.; Watts, P.C. The transcriptome of the novel dinoflagellate Oxyrrhis marina (alveolata: Dinophyceae): Response to salinity examined by 454 sequencing. BMC Genomics 2011, doi:10.1186/1471-2164-12-519.
[67]  Waller, R.F.; Slamovits, C.H.; Keeling, P.J. Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol. Biol. Evol. 2006, 23, 1437–1443.
[68]  Delwiche, C.F.; Palmer, J.D. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 1996, 13, 873–882, doi:10.1093/oxfordjournals.molbev.a025647.
[69]  Morse, D.; Salois, P.; Markovic, P.; Hastings, J.W. A nuclear-encoded form II rubisco in dinoflagellates. Science 1995, 268, 1622–1624.
[70]  Lin, S.; Zhang, H.; Spencer, D.F.; Norman, J.E.; Gray, M.W. Widespread and extensive editing of mitochondrial mRNAs in dinoflagellates. J. Mol. Biol. 2002, 320, 727–739.
[71]  Jackson, C.J.; Norman, J.E.; Schnare, M.N.; Gray, M.W.; Keeling, P.J.; Waller, R.F. Broad genomic and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biol. 2007, doi:10.1186/1741-7007-5-41.
[72]  Zhang, H.; Lin, S. Mitochondrial cytochrome b mRNA editing in dinoflagellates: Possible ecological and evolutionary associations? J. Eukaryot. Microbiol. 2005, 52, 538–545, doi:10.1111/j.1550-7408.2005.00060.x.
[73]  Zhang, H.; Bhattacharya, D.; Lin, S. A three-gene dinoflagellate phylogeny suggests monophyly of prorocentrales and a basal position for Amphidinium and Heterocapsa. J. Mol. Evol. 2007, 65, 463–474, doi:10.1007/s00239-007-9038-4.
[74]  Sanchez-Puerta, M.V.; Lippmeier, J.C.; Apt, K.E.; Delwiche, C.F. Plastid genes in a non-photosynthetic dinoflagellate. Protist 2007, 158, 105–117.
[75]  Lin, S.; Zhang, H.; Gray, M.W. RNA Editing in Dinoflagellates and Its Implications for the Evolutionary History of the Editing Machinery. In RNA and DNA Editing: Molecular Mechanisms and Their Integration into Biological Systems; Smith, H.C., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2008; pp. 280–309.
[76]  Jackson, C.; Gornik, S.; Waller, R. The mitochondrial genome and transcriptome of the basal dinoflagellate Hematodinium sp.: Character evolution within the highly derived mitochondrial genomes of dinoflagellates. Genome Biol. Evol. 2012, 4, 59–72, doi:10.1093/gbe/evr122.
[77]  Williamson, D.H.; Gardner, M.J.; Preiser, P.; Moore, D.J.; Rangachari, K.; Wilson, R.J. The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: New evidence supports a possible rhodophyte ancestry. Mol. Gen. Genet. 1994, 243, 249–252.
[78]  Denny, P.W.; Preiser, P.R.; Rangachari, K.; Roberts, K.; Roy, A.; Whyte, A.; Strath, M.; Moore, D.J.; Moore, P.W.; Williamson, D.H. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 1996, 261, 155–172, doi:10.1006/jmbi.1996.0449.
[79]  Huang, J.; Mullapudi, N.; Sicheritz-Ponten, T.; Kissinger, J.C. A first glimpse into the pattern and scale of gene transfer in the apicomplexa. Int. J. Parasitol. 2004, 34, 265–274, doi:10.1016/j.ijpara.2003.11.025.
[80]  Archibald, J.M. Plastid evolution: Remnant algal genes in ciliates. Curr. Biol. 2008, 18, R663–R665, doi:10.1016/j.cub.2008.06.031.
[81]  Reyes-Prieto, A.; Moustafa, A.; Bhattacharya, D. Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Curr. Biol. 2008, 18, 956–962, doi:10.1016/j.cub.2008.05.042.
[82]  Stelter, K.; El-Sayed, N.M.; Seeber, F. The expression of a plant-type ferredoxin redox system provides molecular evidence for a plastid in the early dinoflagellate Perkinsus marinus. Protist 2007, 158, 119–130, doi:10.1016/j.protis.2006.09.003.
[83]  Matsuzaki, M.; Kuroiwa, H.; Kuroiwa, T.; Kita, K.; Nozaki, H. A cryptic algal group unveiled: A plastid biosynthesis pathway in the oyster parasite Perkinsus marinus. Mol. Biol. Evol. 2008, 25, 1167–1179, doi:10.1093/molbev/msn064.
[84]  Sheiner, L.; Vaidya, A.B.; McFadden, G.I. The metabolic roles of the endosymbiotic organelles of Toxoplasma and Plasmodium spp. Curr. Opin. Microbiol. 2013, 16, 452–458, doi:10.1016/j.mib.2013.07.003.
[85]  Cavalier-smith, T. Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree 1,2. J. Eukaryot. Microbiol. 1999, 46, 347–366, doi:10.1111/j.1550-7408.1999.tb04614.x.
[86]  Patron, N.J.; Rogers, M.B.; Keeling, P.J. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot. Cell 2004, 3, 1169–1175, doi:10.1128/EC.3.5.1169-1175.2004.
[87]  Keeling, P.J. Chromalveolates and the evolution of plastids by secondary endosymbiosis. J. Eukaryot. Microbiol. 2009, 56, 1–8, doi:10.1111/j.1550-7408.2008.00371.x.
[88]  Goldman, J.C.; Dennett, M.R.; Gordin, H. Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J. Plankton Res. 1989, 11, 391–407, doi:10.1093/plankt/11.2.391.
[89]  Hansen, F.C.; Witte, H.J.; Passarge, J. Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: Size selectivity and preference for calcified Emiliania huxleyi cells. Aquat. Microb. Ecol. 1996, 10, 307–313, doi:10.3354/ame010307.
[90]  Jeong, H.J.; Kang, H.; Shim, J.H.; Park, J.K.; Kim, J.S.; Song, J.Y.; Choi, H.J. Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods acartia spp. Mar. Ecol. Prog. Ser. 2001, 218, 77–86, doi:10.3354/meps218077.
[91]  Jeong, H.J.; Kim, J.S.; Yoo, Y.D.; Kim, S.T.; Kim, T.H.; Park, M.G.; Lee, C.H.; Seong, K.A.; Rang, N.S.; Shim, J.H. Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: A potential biological method to control red tides using mass-cultured grazers. J. Eukaryot. Microbiol. 2003, 50, 274–282, doi:10.1111/j.1550-7408.2003.tb00134.x.
[92]  Hammer, A.; Grüttner, C.; Schumann, R. The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina dujardin (dinoflagellate). Protist 1999, 150, 375–382, doi:10.1016/S1434-4610(99)70039-8.
[93]  Hammer, A.; Gruttner, C.; Schumann, R. New biocompatible tracer particles: Use for estimation of microzooplankton grazing, digestion, and growth rates. Aquat. Microb. Ecol. 2001, 24, 153–161, doi:10.3354/ame024153.
[94]  Wootton, E.C.; Zubkov, M.V.; Jones, D.H.; Jones, R.H.; Martel, C.M.; Thornton, C.A.; Roberts, E.C. Biochemical prey recognition by planktonic protozoa. Environ. Microbiol. 2007, 9, 216–222, doi:10.1111/j.1462-2920.2006.01130.x.
[95]  Sieburth, J.M. Acrylic acid, an “antibiotic” principle in phaeocystis blooms in antarctic waters. Science 1960, 132, 676–677.
[96]  Barlow, R.; Burkill, P.; Mantoura, R. Grazing and degradation of algal pigments by marine protozoan Oxyrrhis marina. J. Exp. Mar. Biol. Ecol. 1988, 119, 119–129, doi:10.1016/0022-0981(88)90227-4.
[97]  Flynn, K.J.; Davidson, K.; Cunningham, A. Prey selection and rejection by a microflagellate: Implications for the study and operation of microbial food webs. J. Exp. Mar. Biol. Ecol. 1996, 196, 357–372, doi:10.1016/0022-0981(95)00140-9.
[98]  Monger, B.C.; Landry, M.R.; Brown, S.L. Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol. Oceanogr. 1999, 44, 1917–1927, doi:10.4319/lo.1999.44.8.1917.
[99]  John, E.; Davidson, K. Prey selectivity and the influence of prey carbon: Nitrogen ratio on microflagellate grazing. J. Exp. Mar. Biol. Ecol. 2001, 260, 93–111, doi:10.1016/S0022-0981(01)00244-1.
[100]  Matz, C.; Jurgens, K. Effects of hydrophobic and electrostatic cell surface properties of bacteria on feeding rates of heterotrophic nanoflagellates. Appl. Environ. Microbiol. 2001, 67, 814–820, doi:10.1128/AEM.67.2.814-820.2001.
[101]  Matz, C.; Jürgens, K. High motility reduces grazing mortality of planktonic bacteria. Appl. Environ. Microbiol. 2005, 71, 921–929, doi:10.1128/AEM.71.2.921-929.2005.
[102]  Matz, C.; Boenigk, J.; Arndt, H.; Jürgens, K. Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat. Microb. Ecol. 2002, 27, 137–148, doi:10.3354/ame027137.
[103]  Wolfe, G.V.; Steinke, M.; Kirst, G.O. Grazing-activated chemical defence in a unicellular marine alga. Nature 1997, 387, 894–897.
[104]  Evans, C.; Wilson, W.H. Preferential grazing of Oxyrrhis marina on virus-infected Emiliania huxleyi. Limnol. Oceanogr. 2008, 53, 2035–2040, doi:10.4319/lo.2008.53.5.2035.
[105]  Droop, M.R. Nutritional investigation of phagotrophic protozoa under axenic conditions. Helgol?nder Wiss. Meeresunters. 1970, 20, 272–277.
[106]  Droop, M.R. Water-soluble factors in the nutrition of Oxyrrhis marina. J. Mar. Biol. Assoc. UK 1959, 38, 605–620, doi:10.1017/S0025315400007037.
[107]  Droop, M.R.; Pennock, J.F. Terpenoid quinones and steroids in the nutrition of Oxyrrhis marina. J. Mar. Biol. Assoc. UK 1971, 51, 455–470, doi:10.1017/S002531540003191X.
[108]  ?pik, H.; Flynn, K. The digestive process of the dinoflagellate, Oxyrrhis marina dujardin, feeding on the chlorophyte, Dunaliella primolecta butcher: A combined study of ultrastructure and free amino acids. New Phytol. 1989, 113, 143–151, doi:10.1111/j.1469-8137.1989.tb04700.x.
[109]  Mast, S.; Stahler, N. The relation between luminous intensity, adaptation to light, and rate of locomotion in Amoeba proteus (leidy). Biol. Bull. 1937, 73, 126–133, doi:10.2307/1537874.
[110]  Podesta, A.; Marangoni, R.; Vilani, C.; Colombetti, G. A rhodopsin-like molecule on the plasma membrane of Fabrea salina. J. Eukaryot. Microbiol. 1994, 41, 565–569, doi:10.1111/j.1550-7408.1994.tb01518.x.
[111]  Seibach, M.; Hader, D.P.; Kuhlmann, H.W. Phototaxis in Chlamydodon mnemosyne: Determination of the illuminance-response curve and the action spectrum. J. Photochem. Photobiol. B Biol. 1999, 49, 35–40, doi:10.1016/S1011-1344(99)00013-5.
[112]  Cadetti, L.; Marroni, F.; Marangoni, R.; Kuhlmann, H.-W.; Gioffre, D.; Colombetti, G. Phototaxis in the ciliated protozoan Ophryoglena flava: Dose-effect curves and action spectrum determination. J. Photochem. Photobiol. B Biol. 2000, 57, 41–50, doi:10.1016/S1011-1344(00)00075-0.
[113]  Saranak, J.; Foster, K.W. Photoreceptor for curling behavior in Peranema trichophorum and evolution of eukaryotic rhodopsins. Eukaryot. Cell 2005, 4, 1605–1612, doi:10.1128/EC.4.10.1605-1612.2005.
[114]  Lobban, C.S.; Hallam, S.J.; Mukherjee, P.; Petrich, J.W. Photophysics and multifunctionality of hypericin-like pigments in heterotrich ciliates: A phylogenetic perspective. Photochem. Photobiol. 2007, 83, 1074–1094, doi:10.1111/j.1751-1097.2007.00191.x.
[115]  Fabczak, H.; Sobierajska, K.; Fabczak, S. A rhodopsin immunoanalog in the related photosensitive protozoans Blepharisma japonicum and Stentor coeruleus. Photochem. Photobiol. Sci. 2008, 7, 1041–1045.
[116]  Jakobsen, H.H.; Strom, S.L. Circadian cycles in growth and feeding rates of heterotrophic protist plankton. Limnol. Oceanogr. 2004, 49, 1915–1922, doi:10.4319/lo.2004.49.6.1915.
[117]  Strom, S.L. Light-aided digestion, grazing and growth in herbivorous protists. Aquat. Microb. Ecol. 2001, 23, 253–261, doi:10.3354/ame023253.
[118]  Skovgaard, A. A phagotrophically derivable growth factor in the plastic dinoflagellates Gyrodinium resplendens. J. Phycol. 2000, 36, 1069–1078, doi:10.1046/j.1529-8817.2000.00009.x.
[119]  Jakobsen, H.H.; Hansen, P.J.; Larsen, J. Growth and grazing responses of two chloroplast-retaining dinoflagellates: Effect of irradiance and prey species. Mar. Ecol. Prog. Ser. 2000, 201, 121–128, doi:10.3354/meps201121.
[120]  Li, A.; Stoecker, D.K.; Adolf, J.E. Feeding, pigmentation, photosynthesis and growth of the mixotrophic dinoflagellate Gyrodinium galatheanum. Aquat. Microb. Ecol. 1999, 19, 163–176, doi:10.3354/ame019163.
[121]  Moran, M.A.; Zepp, R.G. Role of photoreactions in the formation of biologically labile compounds from dissolved organic matter. Limnol. Oceanogr. 1997, 42, 1307–1316, doi:10.4319/lo.1997.42.6.1307.
[122]  Klein, B.; Gieskes, W.W.; Krray, G.G. Digestion of chlorophylls and carotenoids by the marine protozoan Oxyrrhis marina studied by HPLC analysis of algal pigments. J. Plankton Res. 1986, 8, 827–836, doi:10.1093/plankt/8.5.827.
[123]  Béja, O.; Aravind, L.; Koonin, E.V.; Suzuki, M.T.; Hadd, A.; Nguyen, L.P.; Jovanovich, S.B.; Gates, C.M.; Feldman, R.A.; Spudich, J.L. Bacterial rhodopsin: Evidence for a new type of phototrophy in the sea. Science 2000, 289, 1902–1906, doi:10.1126/science.289.5486.1902.
[124]  Béja, O.; Spudich, E.N.; Spudich, J.L.; Leclerc, M.; DeLong, E.F. Proteorhodopsin phototrophy in the ocean. Nature 2001, 411, 786–789, doi:10.1038/35081051.
[125]  Lin, S.; Zhang, H.; Zhuang, Y.; Tran, B.; Gill, J. Spliced leader-based metatranscriptomic analyses lead to recognition of hidden genomic features in dinoflagellates. Proc. Natl. Acad. Sci. USA 2010, 107, 20033–20038, doi:10.1073/pnas.1007246107.
[126]  Slamovits, C.H.; Okamoto, N.; Burri, L.; James, E.R.; Keeling, P.J. A bacterial proteorhodopsin proton pump in marine eukaryotes. Nat. Commun. 2011, doi:10.1038/ncomms1188.
[127]  Kent, W.S. A Manual of the Infusoria: Including a Description of All Known Flagellate, Ciliate, and Tentaculiferous Protozoa, British and Foreign, and an Account of the Organization and the Affinities of the Sponges; D. Bogue: London, UK, 1880.
[128]  Senn, G. Oxyrrhis, Nephroselmis und einige Euflagellaten, nebst Bemerkungen uber deren System; Wilhelm Engelmann: Leipzig, Germany, 1911; pp. 604–672.
[129]  Cosson, J.; Cachon, M.; Cachon, J.; Cosson, M.-P. Swimming behaviour of the unicellular biflagellate Oxyrrhis marina: In vivo and in vitro movement of the two flagella. Biol. Cell 1988, 63, 117–126, doi:10.1016/0248-4900(88)90050-0.
[130]  Bartumeus, F.; Peters, F.; Pueyo, S.; Marrasé, C.; Catalan, J. Helical lévy walks: Adjusting searching statistics to resource availability in microzooplankton. Proc. Natl. Acad. Sci. USA 2003, 100, 12771–12775, doi:10.1073/pnas.2137243100.
[131]  Crenshaw, H.C. A new look at locomotion in microorganisms: Rotating and translating. Am. Zool. 1996, 36, 608–618.
[132]  Tarran, G.A. Aspects of Grazing Behaviour of the Marine Dinoflagellate Oxyrrhis marina, Dujardin; University of Southampton: Southampton, UK, 1991.
[133]  Menden-Deuer, S.; Grünbaum, D. Individual foraging behaviors and population distributions of a planktonic predator aggregating to phytoplankton thin layers. Limnol. Oceanogr. 2006, 51, 109–116, doi:10.4319/lo.2006.51.1.0109.
[134]  Grünbaum, D. Predicting availability to consumers of spatially and temporally variable resources. Hydrobiologia 2002, 480, 175–191, doi:10.1023/A:1021296103358.
[135]  Hartz, A.J.; Sherr, B.F.; Sherr, E.B. Using inhibitors to investigate the involvement of cell signaling in predation by marine phagotrophic protists. J. Eukaryot. Microbiol. 2008, 55, 18–21, doi:10.1111/j.1550-7408.2007.00297.x.
[136]  Fenchel, T. Ecology of Protozoa: The Biology of Free-Living Phagotrophic Protists; Springer-Verlag: Madison, WI, USA, 1987.
[137]  H?hfeld, I.; Melkonian, M. Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (Dinophyceae) and its rearrangement during phagocytosis. Protist 1998, 149, 75–88, doi:10.1016/S1434-4610(98)70011-2.
[138]  Barker, H.A. The culture and physiology of the marine dinoflagellates. Arch. Microbiol. 1935, 6, 157–181.
[139]  Flynn, K.J.; Davidson, K. Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina. II. Release of non-protein amines and faeces during predation of isochrysis. J. Plankton Res. 1993, 15, 893–905, doi:10.1093/plankt/15.8.893.
[140]  Bretler, W. Continuous breeding of marine pelagic copepods in the presence of heterotrophic dinoflagellates. Mar. Ecol. Prog. Ser. 1980, 2, 229–233, doi:10.3354/meps002229.
[141]  Hansen, B.; Bj?rnsen, P.K.; Hansen, P.J. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 1994, 39, 395–403, doi:10.4319/lo.1994.39.2.0395.
[142]  Breteler, W.K.; Schogt, N.; Baas, M.; Schouten, S.; Kraay, G. Trophic upgrading of food quality by protozoans enhancing copepod growth: Role of essential lipids. Mar. Biol. 1999, 135, 191–198, doi:10.1007/s002270050616.
[143]  Scott, J. Further nutritional studies on the marine rotifer encentrum linnhei. Rotifer Symp. IV 1987, 42, 303–306, doi:10.1007/978-94-009-4059-8_41.
[144]  Pfiester, L.A.; Anderson, D.M. Dinoflagellate reproduction. In The Biology of Dinoflagellates; Taylor, F.J.R., Ed.; Blackwell Scientific Publications: Hoboken, NJ, USA, 1987; Volume 21, pp. 611–648.
[145]  Whiteley, A.; Burkill, P.; Sleigh, M. Rapid method for cell cycle analysis in a predatory marine dinoflagellate. Cytometry 1993, 14, 909–915, doi:10.1002/cyto.990140809.
[146]  Lin, S.; Mulholland, M.R.; Zhang, H.; Feinstein, T.N.; Jochem, F.J.; Carpenter, E.J. Intense grazing and prey-dependent growth of Pfiesteria piscicida (Dinophyceae). J. Phycol. 2004, 40, 1062–1073, doi:10.1111/j.1529-8817.2004.03217.x.
[147]  Begun, A.; Orlova, T.Y.; Selina, M. A “bloom” in the water of Amursky bay (sea of Japan) caused by the dinoflagellate Oxyrrhis marina dujardin, 1841. Russ. J. Mar. Biol. 2004, 30, 51–55, doi:10.1023/B:RUMB.0000020569.49887.7e.
[148]  Kimmance, S.A.; Atkinson, D.; Montagnes, D.J. Do temperature-food interactions matter? Responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina. Aquat. Microb. Ecol. 2006, 42, 63–73, doi:10.3354/ame042063.
[149]  Jonsson, P.R. Tidal rhythm of cyst formation in the rock pool ciliate Strombidium oculatum gruber (ciliophora, oligotrichida): A description of the functional biology and an analysis of the tidal synchronization of encystment. J. Exp. Mar. Biol. Ecol. 1994, 175, 77–103, doi:10.1016/0022-0981(94)90177-5.
[150]  Anderson, D.M.; Wall, D. Potential importance of benthic cysts of Gonyaulax tamarensis and G. excavata in initiating toxic dinoflagellate blooms. J. Phycol. 1978, 14, 224–234, doi:10.1111/j.1529-8817.1978.tb02452.x.
[151]  Matthiessen, J.; de Vernal, A.; Head, M.; Okolodkov, Y.; Harland, R. Modern organic-walled dinoflagellate cysts in Arctic marine environments and their (paleo-) environmental significance. Pal?ontologische Zeitschrift 2005, 79, 3–51.
[152]  Vink, A.; Zonneveld, K.A.F.; Willems, H. Organic-walled dinoflagellate cysts in western equatorial Atlantic surface sediments: Distribution and their relation to environment. Rev. Palaeobot. Palynol. 2000, 112, 247–286, doi:10.1016/S0034-6667(00)00046-4.
[153]  Wall, D. Biological problems concerning fossilizable dinoflagellates. Geosci. Man 1971, 2, 1–15.
[154]  Droop, M.R. A note on some physical conditions for cultivating Oxyrrhis marina. J. Mar. Biol. Assoc. UK 1959, 38, 599–604, doi:10.1017/S0025315400007025.
[155]  Havskum, H. Effects of small-scale turbulence on interactions between the heterotrophic dinoflagellate Oxyrrhis marina and its prey, Isochrysis sp. Ophelia 2003, 57, 125–135, doi:10.1080/00785236.2003.10409509.
[156]  Pedersen, M.F.; Hansen, P.J. Effects of high pH on the growth and survival of six marine heterotrophic protists. Mar. Ecol. Prog. Ser. 2003, 260, 33–41, doi:10.3354/meps260033.
[157]  Peters, F.; Marrasé, C. Effects of turbulence on plankton: An overview of experimental evidence and some theoretical considerations. Mar. Ecol. Prog. Ser. 2000, 205, 291–306, doi:10.3354/meps205291.
[158]  Davidson, K.; Sayegh, F.; Montagnes, D.J.S. Oxyrrhis marina-based models as a tool to interpret protozoan population dynamics. J. Plankton Res. 2011, 33, 651–663, doi:10.1093/plankt/fbq105.
[159]  Johnson, M. Physical control of plankton population abundance and dynamics in intertidal rock pools. Hydrobiologia 2000, 440, 145–152, doi:10.1023/A:1004106808213.
[160]  Hansson, H.G. South scandinavian marine protoctista. Provisional Check-list Compiled at the Tjarno Marine Biological Laboratory. Available online: http://www.yumpu.com/it/document/view/5925990/south-scandinavian-marine-protoctista-protoctista-tmbl (accessed on 10 October 2013).
[161]  Orlova, T.Y.; Stonik, I.; Shevchenko, O. Flora of planktonic microalgae of Amursky bay, sea of Japan. Russ. J. Mar. Biol. 2009, 35, 60–78, doi:10.1134/S106307400901009X.
[162]  Quevedo, M.; Anado, R. Spring microzooplankton composition, biomass and potential grazing in the central cantabrian coast (southern bay of biscay). Oceanol. Acta 2000, 23, 297–310, doi:10.1016/S0399-1784(00)00128-6.
[163]  Johnson, M.D.; Rome, M.; Stoecker, D.K. Microzooplankton grazing on Prorocentrum minimum and Karlodinium micrum in chesapeake bay. Limnol. Oceanogr. 2003, 48, 238–248, doi:10.4319/lo.2003.48.1.0238.
[164]  Galluzzi, L.; Penna, A.; Bertozzini, E.; Vila, M.; Garces, E.; Magnani, M. Development of a real-time PCR assay for rapid detection and quantification of Alexandrium minutum (a dinoflagellate). Appl. Environ. Microbiol. 2004, 70, 1199–1206, doi:10.1128/AEM.70.2.1199-1206.2004.
[165]  Zhang, H.; Lin, S. Development of a cob-18S rRNA gene real-time PCR assay for quantifying Pfiesteria shumwayae in the natural environment. Appl. Environ. Microbiol. 2005, 71, 7053–7063, doi:10.1128/AEM.71.11.7053-7063.2005.
[166]  Touzet, N.; Keady, E.; Raine, R.; Maher, M. Evaluation of taxa-specific real-time PCR, whole-cell fish and morphotaxonomy analyses for the detection and quantification of the toxic microalgae Alexandrium minutum (Dinophyceae), global clade ribotype. FEMS Microbiol. Ecol. 2009, 67, 329–341, doi:10.1111/j.1574-6941.2008.00627.x.
[167]  Dyhrman, S.T.; Erdner, D.; Du, J.L.; Galac, M.; Anderson, D.M. Molecular quantification of toxic Alexandrium fundyense in the gulf of maine using real-time PCR. Harmful Algae 2006, 5, 242–250, doi:10.1016/j.hal.2005.07.005.
[168]  Hosoi-Tanabe, S.; Sako, Y. Species-specific detection and quantification of toxic marine dinoflagellates Alexandrium tamarense and A. catenella by real-time PCR assay. Mar. Biotechnol. 2005, 7, 506–514, doi:10.1007/s10126-004-4128-4.
[169]  Wang, L.; Zhuang, Y.; Zhang, H.; Lin, X.; Lin, S. DNA barcoding species in Alexandrium tamarense complex using ITS and proposing designation of five species. Harmful Algae 2013. in press.
[170]  Yuan, J.; Mi, T.; Zhen, Y.; Yu, Z. Development of a rapid detection and quantification method of Karenia mikimotoi by real-time quantitative PCR. Harmful Algae 2012, 17, 83–91, doi:10.1016/j.hal.2012.03.004.
[171]  Zhang, H.; Litaker, W.; Vandersea, M.W.; Tester, P.; Lin, S. Geographic distribution of Karlodinium veneficum in the US east coast as detected by ITS-ferredoxin real-time PCR assay. J. Plankton Res. 2008, 30, 905–922, doi:10.1093/plankt/fbn047.
[172]  Bowers, H.A.; Tengs, T.; Glasgow, H.B.; Burkholder, J.M.; Rublee, P.A.; Oldach, D.W. Development of real-time PCR assays for rapid detection of Pfiesteria piscicida and related dinoflagellates. Appl. Environ. Microbiol. 2000, 66, 4641–4648, doi:10.1128/AEM.66.11.4641-4648.2000.
[173]  Mieog, J.C.; van Oppen, M.J.; Berkelmans, R.; Stam, W.T.; Olsen, J.L. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol. Ecol. Resour. 2009, 9, 74–82, doi:10.1111/j.1755-0998.2008.02222.x.

Full-Text

comments powered by Disqus

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133