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Extreme Eukaryotes in the Hydrothermal Environments of Lassen Volcanic National Park

Extreme Eukaryotes in the Hydrothermal Environments of Lassen Volcanic National Park. Gordon Wolfe Dept. Biological Sciences California State University Chico. Outline. My life as a virologist Protist molecular diversity in LVNP hydrothermal sites Possible eukaryotic viral hosts

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Extreme Eukaryotes in the Hydrothermal Environments of Lassen Volcanic National Park

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  1. Extreme Eukaryotes in the Hydrothermal Environments of Lassen Volcanic National Park Gordon Wolfe Dept. Biological Sciences California State University Chico

  2. Outline • My life as a virologist • Protist molecular diversity in LVNP hydrothermal sites • Possible eukaryotic viral hosts • eukaryotes vs. prokaryotes as viral hosts

  3. Oregon State, 1989: marine coccolithophorid alga Emiliania huxleyi ~90 nm hexagonal particles in algal lysate 

  4. Brussaard et al. 1996. Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquatic Microbial Ecology 10: 105

  5. Castberg et al. (2002). Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). J. Phycology 38: 767 Wilson et al. (2005). Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309: 1090

  6. Suttle, 2005. Viruses in the sea. Nature 437: 356

  7. Humans of the world

  8. Protist Molecular Diversity Non-thermal sites Neutral Lakes, rivers and oceans, groundwater Acidic Acid mine drainage Thermal sites Neutral Non-sulfidic hydrothermal Acidic Sulfidic hydrothermal

  9. Rio Tinto, Spain • pH 2; heavy metals • chlorophytes, diatoms • ciliates, amoebae, cercomonads • fungi

  10. 1 = Sulfur works 2 = Bumpass Hell 3 = Devil’s Kitchen 4 = Boiling Springs Lake

  11. Upper Sulfur works: pH 2, 96 oC Bumpass Hell: pH 1.4-3.2 11-68 oC

  12. Questions • What eukaryotic rDNA sequences exist in LVNP hydrothermal environments? • Is genetic diversity dominated by autotrophs or heterotrophs? • What factors determine the composition and diversity of protists in LVNP?

  13. 18S rDNA eubacterial16S rDNA CTAB UC FD USW 123 pH 3.3, 25 C SW114 pH 1.9, 69 C USW 123 pH 3.3, 25 C SW114 pH 1.9, 69 C

  14. Low vs. high18S rRNA RFLP diversity pH 4.6, 37 C pH 1.7, 30 C pH 1.8, 68 C

  15. Baldauf, 2003. The deep roots of eukaryotes. Science 300: 1703

  16. Cyanidium-like alga cultivated from Boiling Springs Lake

  17. Baldauf, 2003. The deep roots of eukaryotes. Science 300: 1703

  18. Baldauf, 2003. The deep roots of eukaryotes. Science 300: 1703

  19. Baldauf, 2003. The deep roots of eukaryotes. Science 300: 1703

  20. Baldauf, 2003. The deep roots of eukaryotes. Science 300: 1703

  21. Observations • Few planktonic forms in streams; most benthic • Photosynthetic acidophiles dominate • Heterotrophic taxa include alveolates, amoebae, flagellates and fungi • Many sequences highly similar to cultured isolates, Rio Tinto clone library • Some unclassified / deeply branching organisms • No clear correspondence between sites, or site conditions, and genetic diversity

  22. BH107: pH 1.8 68 oC

  23. Problems and biases • Incomplete survey • Biases in extraction, amplification and cloning • Are the genes from living organisms? Acknowledgements Patty Siering and Mark Wilson Humboldt State University Rachel Whitaker, Scott Dawson UC Berkeley CSUC graduate students: Patricia Brown CSUC undergraduate students: Mary Ellen Sanders CSUC classes: Microbial Ecology, Microbiology Lassen Volcanic National Park

  24. Trophic Structure in Acidic Hydrothermal Sites What are biotic limits to primary production? Lots of ‘meat on the hoof’: chemosynthesis and photosynthesis At times, high biomass from chemosynthetic environments Factors that might affect viral ecology: abiotic conditions environmental stability host diversity environmental vs. host conditions

  25. Protist virus biology Viruses now known for chlorophytes, stramenopiles, haptophytes, alveolates Suttle, 2005. Viruses in the sea. Nature 437: 356 Some unusually large genomes (300 – 1200 kb) Unusual genes (transcription factors, K ion channels, signal transduction factors)

  26. Baldauf, 2003. The deep roots of eukaryotes. Science 300: 1703

  27. Paramecium bursaria chlorella virus (PBCV-1) large, icosahedral, plaque-forming, dsDNA viruses Chlorella host is a hereditary endosymbiont ofthe ciliate Paramecium bursaria. http://plantpath.unl.edu/facilities/virology/intro.html prototype of a group (family Phycodnaviridae, genus Chlorovirus) NC64A viruses (type = PBCV-1): infect Chlorella-NC64A isolated from Paramecium bursaria originally collected in the southeastern United States. Pbi viruses (type = CVA-1): infect Chlorella-Pbi isolated from Paramecium bursaria originally collected in Germany. Hydra viruses (type = HVCV-1): infect Chlorella originally isolated from Hydra viridis. This alga host was never cultured presumably because the virus is either lysogenic or integrates into the host genome.

  28. Infection of Chlorella strain NC64A by PBCV-1. (A) Viral particle in close proximity to the alga (B and C) Attachment of PBCV-1 to the algal wall and digestion of the wall at the point of attachment (D) Viral DNA beginning to enter the host (E) An empty viral capsid remaining on the surface of the host (F) PBCV-1 attachment and dissolution of a Chlorella cell wall fragment. Note that (i) viral attachment always occurs on the external side of the wall (i.e., the internal side of the wall curls inward) and (ii) DNA is not released from viral particles attached to wall fragments. Size markers in panel E and F represent 100 nm and 200 nm, respectively. http://plantpath.unl.edu/facilities/virology/intro.html • 330,744-bp genome: • multiple DNA methyltransferases and DNA site-specific endonucleases • part, if not the entire machinery to glycosylate glycoproteins • at least two types of introns : a self-splicing intron in a transcription factor-like gene and a splicesomal processed type of intron in its DNA polymerase

  29. Eukaryote vs. prokaryotes as hosts for viruses in acidic thermal sites Eukaryotes: dominant photoautotrophs below pH 4 Cyanidium sp. from BSL One of the smallest known eukaryotic genomes (Cyanidioschyzon merolae: 16.5 Mb)

  30. Messerli et al., 2005. Life at acidic pH imposes an increased energetic cost for a eukaryotic acidophile. J. Exp. Biol. 208: 2569 Cytosolic pH of acidophilic eukaryotes is ~neutral

  31. pH 2 pH 6 pH 2 pH 6

  32. Conclusions • Hydrothermal systems are highly dynamic, variable over time and space, and contain multiple habitats • Diverse protist communities in LVNP hydrothermal sites: likely viral hosts • Impact of viruses on hydrothermal acidophilic eukaryotes completely unknown. Work in other aquatic systems suggests likely impact.

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