Microbial Ecology

, Volume 66, Issue 4, pp 823–830 | Cite as

Abundance and Novel Lineages of Thraustochytrids in Hawaiian Waters

Environmental Microbiology


Thraustochydrids has been known for their ubiquitous distribution in the ocean. However, a few efforts have been made to investigate their ecology. In this study, we have applied molecular method, acriflavine direct detection, and classical oceanographic methods to investigate the abundance and diversity of thraustochytrids in the North Pacific subtropical gyre. Our results revealed interesting temporal and spatial variations of their population. Out of three seasons (spring, summer, and fall), cruise Hawaii Ocean Time-series (HOT)-216 during November 2009 obtained the highest abundance of thraustochytrids ranging from 1,890 (Station S1C1, 45 m) to 630,000 (Station S2C12, 100 m) cells L−1 of seawater, which accounted for a 0.79 to 281.0 % biomass ratio to that of bacteria in terms of gram carbon per liter. A patchy distribution of these organisms was widely observed in the water column and they were somehow related to the maximum chlorophyll layers. A total of 25 operational taxonomic units (OTUs) from cruise HOT-216 formed four phylogroups in the specific labyrinthulomycetes 18S rRNA-based phylogenetic tree, with the largest group of 20 OTUs fell into the Aplanochytrium cluster and the others aligned with uncultured clones or none, thus appeared to be undescribed. This study indicates the presence of new thraustochytrids lineages and their quantitative importance in the marine water column.


Euphotic Zone Station S1C1 North Pacific Subtropical Gyre Oceanographic Parameter Hawaiian Water 



This work was partially funded by National Natural Science Foundation of China grant 31170109 (GYW) and NOAA grants NA04OAR4600196(GYW) and NA09AOR4170060 (GYW). We thank the Hawaii Ocean Time-series observations program for their support during the sampling efforts and for allowing physical oceanographic data access during our results analysis.

Supplementary material

248_2013_275_MOESM1_ESM.doc (203 kb)
ESM 1 (DOC 203 kb)


  1. 1.
    Raghukumar S, Schaumann K (1993) An epifluorescence microscopy method for direct detection and enumeration of the fungi-like marine protists, the thraustochytrids. Limnol Oceanogr 38(l):182–187CrossRefGoogle Scholar
  2. 2.
    Fan KW, Vrijmoed LLP, Jones EBG (2002) Zoospore chemotaxis of mangrove thraustochytrids from Hong Kong. Mycologia 94:569–578CrossRefPubMedGoogle Scholar
  3. 3.
    Raghukumar S (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur J Protistol 38:127–145CrossRefGoogle Scholar
  4. 4.
    Leander CL, Porter D, Leander BS (2004) Comparative morphology and molecular phylogeny of aplanochytrids (Labyrinthulomycota). Eur J Protistol 40:317–328CrossRefGoogle Scholar
  5. 5.
    Raghukumar S, Damare VS (2011) Increasing evidence for the important role of Labyrinthulomycetes in marine ecosystems. Bot Mar 54(1):3–11CrossRefGoogle Scholar
  6. 6.
    Raghukumar S, Sharma S, Raghukumar C, Sathe-Pathak V (1994) Thraustochytrid and fungal component of marine detritus. IV. Laboratory studies on decomposition of leaves of the mangrove Rhizophora apiculata Blume. J Exp Mar Biol Ecol 183:113–131CrossRefGoogle Scholar
  7. 7.
    Bremer GB, Talbot G (1995) Cellulolytic enzyme activity in the marine protist Schizochytrium aggregatum. Bot Mar 38:37–41CrossRefGoogle Scholar
  8. 8.
    Damare V, Raghukumar S (2008) Abundance of thraustochytrids and bacteria in the equatorial Indian Ocean, in relation to transparent exopolymeric particles (TEPs). FEMS Microbiol Ecol 65:40–49CrossRefPubMedGoogle Scholar
  9. 9.
    Bongiorni L, Dini F (2002) Distribution and abundance of thraustochytrids in different Mediterranean coastal habitats. Aquat Microb Ecol 30:49–56CrossRefGoogle Scholar
  10. 10.
    Naganuma T, Takasugi H, Kimura H (1998) Abundance of thraustochytrids in coastal plankton. Mar Ecol Prog Ser 162:105–110CrossRefGoogle Scholar
  11. 11.
    Cavalier-Smith T, Chao EEY (2006) Phylogeny and megasystematics of phagotrophic heterokonts (Kingdom Chromista). J Mol Evol 62:388–420CrossRefPubMedGoogle Scholar
  12. 12.
    Yokoyama R, Honda D (2007) Taxonomic rearrangement of the genus Schizochytrium sensu lato based on morphology, chemotaxonomic characteristics, and 18S rRNA gene phylogeny (Thraustochytriaceae, Labyrinthulomycetes): emendation for Schizochytrium and erection of Aurantiochytrium and Oblongichytrium gen. nov. Mycoscience 48:199–211CrossRefGoogle Scholar
  13. 13.
    Yokoyama R, Salleh B, Honda D (2007) Taxonomic rearrangement of the genus Ulkenia sensu lato based on morphology, chemotaxonomical characteristics, and 18S rRNA gene phylogeny (Thraustochytriaceae, Labyrinthulomycetes): emendation for Ulkenia and erection of Botryochytrium, Parietichytrium, and Sicyoidochytrium gen. nov. Mycoscience 48:329–341CrossRefGoogle Scholar
  14. 14.
    Tsui CKM, Marshall W, Yokoyama R, Honda D et al (2009) Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding. Mol Phylogenet Evol 50:129–140CrossRefPubMedGoogle Scholar
  15. 15.
    Dick MW (2001) Straminipilous fungi: systematics of the peronosporomycetes including accounts of the marine straminipilous protists, the plasmodiophorids and similar organisms. Kluwer, DordrechtCrossRefGoogle Scholar
  16. 16.
    Leander CA, Porter D (2001) The Labyrinthulomycota is comprised of three distinct lineages. Mycologia 93:459–464CrossRefGoogle Scholar
  17. 17.
    Stoeck T, Epstein S (2003) Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments. Appl Environ Microbiol 69:2657–2663PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Lovejoy C, Massana R, Pedro's-Alio' C (2006) Diversity and distribution of marine microbial eukaryotes in the Arctic Ocean and adjacent Seas. Appl Environ Microbiol 72:3085–3095PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Collado-Mercado E, Radway JC (2010) Novel uncultivated labyrinthulomycetes revealed by 18S rDNA sequences from seawater and sediment samples. Aquat Microb Ecol 58:215–228CrossRefGoogle Scholar
  20. 20.
    Karl DM, Lukas R (1996) The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep-Sea Res II 43(2–3):129–156CrossRefGoogle Scholar
  21. 21.
    Karl DM, Bidigare RR, Letelier RM (2001) Long-term changes in plankton community structure and productivity in the North Pacific Subtropical Gyre: the domain shift hypothesis. Deep-Sea Res II 48:1449–1470CrossRefGoogle Scholar
  22. 22.
    Letelier RM, Karl DM, Abbott MR, Bidigare RR (2004) Light driven seasonal patterns of Chl and nitrate in the lower euphotic zone of the North Pacific Subtropical Gyre. Limnol Oceanogr 49:508–519CrossRefGoogle Scholar
  23. 23.
    Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25(5):943–948CrossRefGoogle Scholar
  24. 24.
    Kimura H, Fukura T, Naganuma T (1999) Biomass of thraustochytrid protoctists in coastal water. Mar Ecol Prog Ser 189:27–33CrossRefGoogle Scholar
  25. 25.
    Kimura H, Naganuma T (2001) Thraustochytrids: a neglected agent of the marine microbial food chain. Aquat Ecosyst Health Manag 4(1):13–18CrossRefGoogle Scholar
  26. 26.
    Christian JR, Karl DM (1994) Microbial community structure at the US-JGOFS Station ALOHA: inverse methods for estimating biochemical indicator ratios. J Geophys Res 99:14269–14276CrossRefGoogle Scholar
  27. 27.
    Stokes NA, Calvo LMR, Reece KS, Burreson EM (2002) Molecular diagnostics, field validation, and phylogenetic analysis of Quahog Parasite Unknown (QPX), a pathogen of the hard clam Mercenaria mercenaria. Dis Aquat Org 52:233–247CrossRefPubMedGoogle Scholar
  28. 28.
    Caron DA, Countway PD, Savai P et al (2009) Defining DNA-based operational taxonomic units for microbial-eukaryote ecology. Appl Environ Microbiol 75(18):5797–5808PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405CrossRefPubMedGoogle Scholar
  31. 31.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Wuyts J, Perriere G, Van de Peer Y (2004) The European ribosomal RNA database. Nucleic Acids Res 32:101–103CrossRefGoogle Scholar
  33. 33.
    Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704CrossRefPubMedGoogle Scholar
  34. 34.
    Gao Z, Johnson ZI, Wang G (2010) Molecular characterization of the spatial diversity and novel lineages of mycoplankton in Hawaiian coastal waters. ISME J 4:111–120CrossRefPubMedGoogle Scholar
  35. 35.
    Damare V, Raghukumar S (2010) Association of the stramenopilan protists, the aplanochytrids, with zooplankton of the equatorial Indian Ocean. Mar Ecol Prog Ser 399:53–68CrossRefGoogle Scholar
  36. 36.
    Raghukumar S, Ramaiah N, Raghukumar C (2001) Dynamics of thraustochytrid protists in the water column of the Arabian Sea. Aquat Microb Ecol 24:175–186CrossRefGoogle Scholar
  37. 37.
    Gaertner A, Raghukumar S (1980) Ecology of thraustochytrids (lower marine fungi) in the Fladen Ground and other parts of the North Sea. I. ‘Meteor’ Forsch Ergebn A 22:165–185Google Scholar
  38. 38.
    Hebel DV, Karl DM (2001) Seasonal, interannual and decadal variations in particulate matter concentrations and composition in the subtropical North Pacific Ocean. Deep-Sea Res II 48:1669–1695CrossRefGoogle Scholar
  39. 39.
    Scharek R, Latasa M, Karl DM, Bidigare RR (1999) Temporal variations in diatom abundance and downward vertical flux in the oligotrophic North Pacific gyre. Deep-Sea Res I 46:1051–1075CrossRefGoogle Scholar
  40. 40.
    Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG (2004) The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol Oceanogr 49:997–1005CrossRefGoogle Scholar
  41. 41.
    Cienkowski L (1867) Ueber den Bau und die Entwicklung der Labyrinthuleen. Max Schultze's Arch Mikros Anat 3:274–310CrossRefGoogle Scholar
  42. 42.
    Massana R, Castresana J, Balague V, Guillou L et al (2004) Phylogenetic and ecological analysis of novel marine stramenopiles. Appl Environ Microbiol 70:3528–3534PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607CrossRefPubMedGoogle Scholar
  44. 44.
    Damare V, Raghukumar S (2006) Morphology and physiology of the marine straminipilan fungi, the aplanochytrids isolated from the equatorial Indian Ocean. Indian J Mar Sci 35:326–340Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.State Key Laboratory of Marine Environmental ScienceXiamen UniversityXiamenChina
  2. 2.School of Environmental Science and EngineeringTianjin UniversityTianjinChina
  3. 3.Department of MicrobiologyUniversity of Hawaii at ManoaHonoluluUSA

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