1887

Abstract

Diversity of the anaerobic Heterolobosea (Excavata: Discoba) is only poorly understood, especially in marine environments. We have isolated and cultured 16 strains of anaerobic heteroloboseid amoebae and flagellates from brackish, marine and saline anoxic habitats worldwide. Phylogenetic analyses of SSU rDNA sequences and light-microscopic observations showed that all the strains belong to the family Psalteriomonadidae, the main anaerobic lineage of Heterolobosea, and that they represent eight species from the genera , and Seven species are newly isolated and described here as n. sp., n. sp., n. sp., n. sp., n. sp., n. sp. and n. sp. Amoebae, cysts and the ultrastructure of the genus are presented for the first time.

Funding
This study was supported by the:
  • Czech Science Foundation (Award P506/11/1317)
  • Charles University (Award 301711)
  • Charles University (Award SVV 260 087/2014)
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2014-07-01
2024-04-18
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References

  1. Adl S. M., Simpson A. G. B., Farmer M. A., Andersen R. A., Anderson O. R., Barta J. R., Bowser S. S., Brugerolle G., Fensome R. A. & other authors ( 2005 ). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. . J Eukaryot Microbiol 52, 399451. [View Article] [PubMed]
    [Google Scholar]
  2. Amaral Zettler L. A., Gómez F., Zettler E., Keenan B. G., Amils R., Sogin M. L. ( 2002 ). Eukaryotic diversity in Spain’s river of fire. . Nature 417, 137. [View Article] [PubMed]
    [Google Scholar]
  3. Amaral-Zettler L. A., Zettler E. R., Theroux S. M., Palacios C., Aguilera A., Amils R. ( 2011 ). Microbial community structure across the tree of life in the extreme Río Tinto. . ISME J 5, 4250. [View Article] [PubMed]
    [Google Scholar]
  4. Barberà M. J., Ruiz-Trillo I., Tufts J. Y., Bery A., Silberman J. D., Roger A. J. ( 2010 ). Sawyeria marylandensis (Heterolobosea) has a hydrogenosome with novel metabolic properties. . Eukaryot Cell 9, 19131924. [View Article] [PubMed]
    [Google Scholar]
  5. Baumgartner M., Eberhardt S., De Jonckheere J. F., Stetter K. O. ( 2009 ). Tetramitus thermacidophilus n. sp., an amoeboflagellate from acidic hot springs. . J Eukaryot Microbiol 56, 201206. [View Article] [PubMed]
    [Google Scholar]
  6. Bernard C., Simpson A. G. B., Patterson D. J. ( 2000 ). Some free-living flagellates (Protista) from anoxic habitats. . Ophelia 52, 113142. [View Article]
    [Google Scholar]
  7. Broers C. A. M., Stumm C. K., Vogels G. D., Brugerolle G. ( 1990 ). Psalteriomonas lanterna gen. nov., sp. nov., a free-living amoeboflagellate isolated from freshwater anaerobic sediments. . Eur J Protistol 25, 369380. [View Article] [PubMed]
    [Google Scholar]
  8. Broers C. A. M., Meijers H. H. M., Symens J. C., Stumm C. K., Vogels G. D., Brugerolle G. ( 1993 ). Symbiotic association of Psalteriomonas vulgaris n. spec. with Methanobacterium formicicum . . Eur J Protistol 29, 98105. [View Article] [PubMed]
    [Google Scholar]
  9. Brown S., De Jonckheere J. F. ( 1999 ). A reevaluation of the amoeba genus Vahlkampfia based on SSU rDNA sequences. . Eur J Protistol 35, 4954. [View Article]
    [Google Scholar]
  10. Brown M. W., Silberman J. D., Spiegel F. W. ( 2012 ). A contemporary evaluation of the acrasids (Acrasidae, Heterolobosea, Excavata). . Eur J Protistol 48, 103123. [View Article] [PubMed]
    [Google Scholar]
  11. Brugerolle G., Simpson A. G. B. ( 2004 ). The flagellar apparatus of heteroloboseans. . J Eukaryot Microbiol 51, 96107. [View Article] [PubMed]
    [Google Scholar]
  12. Cavalier-Smith T. ( 1993 ). Kingdom protozoa and its 18 phyla. . Microbiol Rev 57, 953994.[PubMed]
    [Google Scholar]
  13. Cavalier-Smith T., Nikolaev S. ( 2008 ). The zooflagellates Stephanopogon and Percolomonas are a clade (class Percolatea: Phylum Percolozoa). . J Eukaryot Microbiol 55, 501509. [View Article] [PubMed]
    [Google Scholar]
  14. de Graaf R. M., Duarte I., van Alen T. A., Kuiper J. W. P., Schotanus K., Rosenberg J., Huynen M. A., Hackstein J. H. P. ( 2009 ). The hydrogenosomes of Psalteriomonas lanterna . . BMC Evol Biol 9, 287. [View Article] [PubMed]
    [Google Scholar]
  15. De Jonckheere J. F. ( 2002 ). A century of research on the amoeboflagellate genus Naegleria . . Acta Protozool 41, 309342.
    [Google Scholar]
  16. De Jonckheere J. F., Baumgartner M., Opperdoes F. R., Stetter K. O. ( 2009 ). Marinamoeba thermophila, a new marine heterolobosean amoeba growing at 50 °C. . Eur J Protistol 45, 231236. [View Article] [PubMed]
    [Google Scholar]
  17. De Jonckheere J. F., Baumgartner M., Eberhardt S., Opperdoes F. R., Stetter K. O. ( 2011a ). Oramoeba fumarolia gen. nov., sp. nov., a new marine heterolobosean amoeboflagellate growing at 54 °C. . Eur J Protistol 47, 1623. [View Article] [PubMed]
    [Google Scholar]
  18. De Jonckheere J. F., Murase J., Opperdoes F. R. ( 2011b ). A new thermophilic heterolobosean amoeba, Fumarolamoeba ceborucoi, gen. nov., sp. nov., isolated near a fumarole at a volcano in Mexico. . Acta Protozool 50, 4148.
    [Google Scholar]
  19. Fenchel T., Patterson D. J. ( 1986 ). Percolomonas cosmopolitus (Ruinen) n. gen., a new type of filter feeding flagellate from marine plankton. . J Mar Biol Assoc UK 66, 465482. [View Article]
    [Google Scholar]
  20. Fulton C. ( 1993 ). A research partner for cell and developmental biology1. . J Eukaryot Microbiol 40, 520532. [View Article]
    [Google Scholar]
  21. Garstecki T., Brown S., De Jonckheere J. F. ( 2005 ). Description of Vahlkampfia signyensis n. sp. (Heterolobosea), based on morphological, ultrastructural and molecular characteristics. . Eur J Protistol 41, 119127. [View Article]
    [Google Scholar]
  22. Hall T. A. ( 1999 ). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. . Nucleic Acids Symp Ser 41, 9598.
    [Google Scholar]
  23. Harding T., Brown M. W., Plotnikov A., Selivanova E., Park J. S., Gunderson J. H., Baumgartner M., Silberman J. D., Roger A. J., Simpson A. G. B. ( 2013 ). Amoeba stages in the deepest branching heteroloboseans, including Pharyngomonas: evolutionary and systematic implications. . Protist 164, 272286. [View Article] [PubMed]
    [Google Scholar]
  24. Katoh K., Misawa K., Kuma K., Miyata T. ( 2002 ). mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. . Nucleic Acids Res 30, 30593066. [View Article] [PubMed]
    [Google Scholar]
  25. Lara E., Chatzinotas A., Simpson A. G. B. ( 2006 ). Andalucia (n. gen.)–the deepest branch within jakobids (Jakobida; Excavata), based on morphological and molecular study of a new flagellate from soil. . J Eukaryot Microbiol 53, 112120. [View Article] [PubMed]
    [Google Scholar]
  26. Lee J. ( 2010 ). De novo formation of basal bodies during cellular differentiation of Naegleria gruberi: progress and hypotheses. . Semin Cell Dev Biol 21, 156162. [View Article] [PubMed]
    [Google Scholar]
  27. Medlin L., Elwood H. J., Stickel S., Sogin M. L. ( 1988 ). The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. . Gene 71, 491499. [View Article] [PubMed]
    [Google Scholar]
  28. Moestrup Ø. ( 2000 ). The flagellate cytoskeleton: introduction of a general terminology for microtubular flagellar roots in protists. . In The Flagellates: Unity, Diversity and Evolution, pp. 6994. Edited by Green J. C., Leadbeater B. S. C. . London:: Taylor & Francis;.
    [Google Scholar]
  29. Murtagh G. J., Dyer P. S., Rogerson A., Nash G. V., Laybourn-Parry J. ( 2002 ). A new species of Tetramitus in the benthos of a saline antarctic lake. . Eur J Protistol 37, 437443. [View Article]
    [Google Scholar]
  30. Nie D. ( 1950 ). Morphology and taxonomy of the intestinal protozoa of the guinea-pig, Cavia porcella . . J Morphol 86, 381493. [View Article] [PubMed]
    [Google Scholar]
  31. Nikolaev S. I., Mylnikov A. P., Berney C., Fahrni J., Pawlowski J., Aleshin V. V., Petrov N. B. ( 2004 ). Molecular phylogenetic analysis places Percolomonas cosmopolitus within Heterolobosea: evolutionary implications. . J Eukaryot Microbiol 51, 575581. [View Article] [PubMed]
    [Google Scholar]
  32. O’Kelly C. J., Silberman J. D., Amaral Zettler L. A., Nerad T. A., Sogin M. L. ( 2003 ). Monopylocystis visvesvarai n. gen., n. sp. and Sawyeria marylandensis n. gen., n. sp.: two new amitochondrial heterolobosean amoebae from anoxic environments. . Protist 154, 281290. [View Article] [PubMed]
    [Google Scholar]
  33. Page F. C., Blanton R. L. ( 1985 ). The Heterolobosea (Sarcodina: Rhizopoda), a new class uniting Schizopyrenida and the Acrasidae (Acrasida). . Protistologica (Paris) 21, 121132.
    [Google Scholar]
  34. Pánek T., Čepička I. ( 2012 ). Diversity of Heterolobosea. . In Genetic Diversity of Microorganisms, pp. 326. Edited by Caliskan M. . Rijeka:: InTech;. [View Article]
    [Google Scholar]
  35. Pánek T., Silberman J. D., Yubuki N., Leander B. S., Cepicka I. ( 2012 ). Diversity, evolution and molecular systematics of the Psalteriomonadidae, the main lineage of anaerobic/microaerophilic heteroloboseans (excavata: discoba). . Protist 163, 807831. [View Article] [PubMed]
    [Google Scholar]
  36. Park J. S., Simpson A. G. B. ( 2011 ). Characterization of Pharyngomonas kirbyi ( =  “Macropharyngomonas halophila” nomen nudum), a very deep-branching, obligately halophilic heterolobosean flagellate. . Protist 162, 691709. [View Article] [PubMed]
    [Google Scholar]
  37. Park J. S., Simpson A. G. B., Lee W. J., Cho B. C. ( 2007 ). Ultrastructure and phylogenetic placement within Heterolobosea of the previously unclassified, extremely halophilic heterotrophic flagellate Pleurostomum flabellatum (Ruinen 1938). . Protist 158, 397413. [View Article] [PubMed]
    [Google Scholar]
  38. Park J. S., Simpson A. G. B., Brown S., Cho B. C. ( 2009 ). Ultrastructure and molecular phylogeny of two heterolobosean amoebae, Euplaesiobystra hypersalinica gen. et sp. nov. and Tulamoeba peronaphora gen. et sp. nov., isolated from an extremely hypersaline habitat. . Protist 160, 265283. [View Article] [PubMed]
    [Google Scholar]
  39. Park J. S., De Jonckheere J. F., Simpson A. G. B. ( 2012 ). Characterization of Selenaion koniopes n. gen., n. sp., an amoeba that represents a new major lineage within heterolobosea, isolated from the Wieliczka salt mine. . J Eukaryot Microbiol 59, 601613. [View Article] [PubMed]
    [Google Scholar]
  40. Perty M. ( 1852 ). Zur Kenntniss kleinster Lebensformen nach Bau, Funktionen, Systematik: mit Specialverzeichniss der in der Schweiz beobachteten. Bern, Switzerland:: Jent & Reinert;.
    [Google Scholar]
  41. Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., Larget B., Liu L., Suchard M. A., Huelsenbeck J. P. ( 2012 ). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. . Syst Biol 61, 539542. [View Article] [PubMed]
    [Google Scholar]
  42. Ruinen J. ( 1938 ). Notizen über Salzflagellaten. II. Über die Verbreitung der Salzflagellaten. . Archiv für Protistenkunde 90, 210258.
    [Google Scholar]
  43. Simpson A. G. B. ( 2003 ). Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). . Int J Syst Evol Microbiol 53, 17591777. [View Article] [PubMed]
    [Google Scholar]
  44. Simpson A. G. B., Patterson D. J. ( 2001 ). On core jakobids and excavate taxa: the ultrastructure of Jakoba incarcerata . . J Eukaryot Microbiol 48, 480492. [View Article] [PubMed]
    [Google Scholar]
  45. Smirnov A. V., Fenchel T. ( 1996 ). Vahlkampfia anaerobica n. sp. and Vannella peregrinia n. sp. (Rhizopoda): anaerobic amoebae from a marine sediment. . Archiv für Protistenkunde 147, 189198. [View Article]
    [Google Scholar]
  46. Stamatakis A. ( 2006 ). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. . Bioinformatics 22, 26882690. [View Article] [PubMed]
    [Google Scholar]
  47. Walsh C. J. ( 2007 ). The role of actin, actomyosin and microtubules in defining cell shape during the differentiation of Naegleria amebae into flagellates. . Eur J Cell Biol 86, 8598. [View Article] [PubMed]
    [Google Scholar]
  48. Yubuki N., Leander B. S. ( 2008 ). Ultrastructure and molecular phylogeny of Stephanopogon minuta: an enigmatic microeukaryote from marine interstitial environments. . Eur J Protistol 44, 241253. [View Article] [PubMed]
    [Google Scholar]
  49. Yubuki N., Simpson A. G. B., Leander B. S. ( 2013 ). Comprehensive ultrastructure of Kipferlia bialata provides evidence for character evolution within the Fornicata (Excavata). . Protist 164, 423439. [View Article] [PubMed]
    [Google Scholar]
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