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The Cyanidiales: Ecology, Biodiversity, and Biogeography

  • Richard W. Castenholz
  • Timothy R. McDermott
Chapter
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 13)

Abstract

The order Cyanidiales (or class Cyanidiophyceae) is comprised of asexual, unicellular red algae that are known to grow in low pH environments (0.2–3.5 or 4.0) and at moderately high temperatures (up to 56°C) and are typically found in acidic geothermal habitats throughout the Earth. No other photosynthetic microorganisms are known to inhabit this combination of conditions. The order Cyanidiales, since 1981, is thought to consist of three genera: Cyanidium, Galdieria, and Cyanidioschyzon (Ciniglia et al., 2004; Gross et al., 2001; Heilmann and Gross, 2001). This group of algae appears to be phylogenetically quite distinct from the main line of descent in the red algae and branches off quite early in geologic time (i.e. ∼ 1.3–1.4 Ga), based on phylogenetic, molecular clock inference and fossil evidence for the first reputed macroalgae, which are presumed to be ancestors of the Rhodophyta (Yoon et al., 2002, 2004, 2006b). In this chapter, we comment on the ecology, biodiversity, and biogeography of these fascinating eukaryotic extremophiles, attempting to assimilate recent, important developments in our understanding of these algae.

Keywords

Acidic algae allophycocyanin antimony arsenic carotenoids chlorophyll a c-phycocyanin copper cultivation Cyanidium Cyanidiales Cyanidioschyzon extremophiles endolithic endosymbion geothermal heavy metals low pH mat decline phototrophs red algae Rhodophyta Galdieria Iceland Japan mercury New Zealand UV radiation Yellowstone 

Notes

Acknowledgments

Support for writing of this paper was from NSF Microbial Interactions and Processes (MCB-0702177). The unpublished sequence work of Elizabeth Perry for the Icelandic isolates is gratefully acknowledged.

References

  1. Albertano, P. and Pinto, G. (1986) The action of heavy metals on the growth of three acidophilic algae. Boll. Soc. Natur. Napoli 95: 319–328.Google Scholar
  2. Albertano, P., Ciniglia, C., Pinto, G. and Pollio, A. (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433: 137–143.CrossRefGoogle Scholar
  3. Allen, M.B. (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch. Mikrobiol. 32: 270–277.PubMedCrossRefGoogle Scholar
  4. Bailey, R.W. and Staehelin, L.A. (1968) The chemical composition of isolated cell walls of Cyanidium caldarium. J. Gen. Microbiol. 54: 269–276.PubMedGoogle Scholar
  5. Barbier, G., Oesterhelt, C., Larson, M.D., Halgren, R.G., Wilkerson, C., Garavito, C., Benning, R.M. and Weber, A.P. (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol. 137: 460–474.PubMedCrossRefGoogle Scholar
  6. Bhaya, D., Grossman, A.R., Steunou, A.-S., Khuri, N., Cohan, F.M., Hamamura, N. et al. (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J. 1: 703–713.PubMedCrossRefGoogle Scholar
  7. Brock, T.D. (1978) Thermophilic Microorganisms and Life at High Temperatures. Springer, New York, USA.CrossRefGoogle Scholar
  8. Ciniglia, C., Yoon, H.S., Pollio, A., Pinto, G., and Bhattacharya, D. (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol. Ecol. 13: 1827–1838.PubMedCrossRefGoogle Scholar
  9. Cockell, C.S. and Rothschild, L.J. (1999) The effects of UV radiation A and B in diurnal variation in photosynthesis in three taxonomically and ecologically diverse microbial mats. Photochem. Photobiol. 69: 203–210.PubMedCrossRefGoogle Scholar
  10. Copeland, J.J. (1936) Yellowstone thermal myxophyceae. Annal. New York Acad. Sci. 36: 1–232.CrossRefGoogle Scholar
  11. De Luca, P. and Moretti, A. (1983) Floridosides in Cyanidium caldarium, Cyanidioschyzon merolae and Galdieria sulphuraria (Rhodophyta, Cyanidiophyceae). J. Phycol. 19: 368–369.CrossRefGoogle Scholar
  12. Doemel, T.D. and Brock, T.D. (1971) The physiological ecology of Cyanidium caldarium. J. Gen. Microbiol. 67: 17–32.Google Scholar
  13. Ferris, M.J., Magnuson, T.S., Fagg, J.A., Thar, R., Kuhl, M., Sheehan, K.B. and Henson, J.M. (2003) Microbially mediated sulphide production in a thermal, acidic algal mat community in Yellowstone National Park. Environ. Microbiol. 5: 954–960.PubMedCrossRefGoogle Scholar
  14. Ferris, M.J., Sheehan, K.B., Kühl, M., Cooksey, K., Wigglesworth-Cooksey, B., Harvey, R. and Henson, J.M. (2005) Algal species and light microenvironment in a low-pH, geothermal microbial mat community. Appl. Environ. Microbiol. 71: 64–71.CrossRefGoogle Scholar
  15. Geitler, L. (1933) Diagnoses neuer Blaualgen von den Sunda-Insela. Arch. Hydrobiol. Suppl. 12: 622–634.Google Scholar
  16. Gross, W. (2000) Ecophysiology of algae living in highly acidic environments. Hydrobiologia 33: 31–37.CrossRefGoogle Scholar
  17. Gross, W. and Gross, S. (2001) Physiological characterization of the acidophilic red alga Galdieria sulphuraria isolated from a mining area. Nova Hedwigia, Beiheft 123: 523–530.Google Scholar
  18. Gross, W. and Oesterhelt, C. (1999) Ecophysiological studies of the red alga Galdieria sulphuraria isolated from southwest Iceland. Plant Biol. 1: 694–700.CrossRefGoogle Scholar
  19. Gross, W. and Schnarrenberger, C. (1995) Heterotrophic growth of two strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol. 36: 633–638.Google Scholar
  20. Gross, W., Heilmann, I., Lenze, D. and Schnarrenberger, C. (2001) Biogeography of the Cyanidiaceae (Rhodophyta) based on 18S ribosomal RNA sequence data. Eur. J. Phycol. 36: 275–280.CrossRefGoogle Scholar
  21. Gross, W., Oesterhelt, C., Tischendorf, G. and Lederer, F. (2002) Charaterization of a non-thermophilic strain of the red algal genus Galdieria isolated from Soos (Czech Rebublic). Eur. J. Phycol. 37: 477–482.CrossRefGoogle Scholar
  22. Heilmann, I. and Gross, W. (2001) Genetic diversity of thermo-acidophilic red algae according to random amplified polymorphic DNA (RAPD) analysis. Nova Hedwigia Beiheft 123: 531–539.Google Scholar
  23. Holm-Hanson, O., Lubin, D., and Helbling, E.W. (1993) Ultraviolet radiation and its effects on organisms in aquatic environments, In A.R. Young, L. Bjorn, J. Mohan, and W. Nultsch (eds.) Environmental UV Photobiology. Plenum Press, New York.Google Scholar
  24. Jackson, C.R., Langner, H.W., Donahoe-Christiansen, J., Inskeep, W.P. and McDermott, T.R. (2001) Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ. Microbiol. 3: 532–542.PubMedCrossRefGoogle Scholar
  25. Kallas, T. and Castenholz, R.W. (1982a) Internal pH and ATP-ADP pools in the cyanobacterium, Synechococcus sp. during exposure to growth-inhibiting low pH. J. Bacteriol. 149: 229–236.PubMedGoogle Scholar
  26. Kallas, T. and Castenholz, R.W. (1982b) Rapid transient growth at low pH in the cyanobacterium Synechococcus sp. J. Bacteriol. 149: 237–246.PubMedGoogle Scholar
  27. Lehr, C.R., Frank, S.D., Norris, T.B., D’Imperio, S., Kalinin, A.V., Toplin, J.A., Castenholz, R.W. and McDermott, T.R. (2007a) Cyanidia (Cyanidiales) population diversity and dynamics in an acid-sulfate chloride spring in Yellowstone National Park. J. Phycol. 43: 3–14.CrossRefGoogle Scholar
  28. Lehr, C.R., Kashyap, D.R. and McDermott, T.R. (2007) New insights into microbial oxidation of arsenic and antimony oxidation. Appl. Environ. Microbiol. 73: 2386–2389.PubMedCrossRefGoogle Scholar
  29. Lin, S., Offner, G.D. and Troxler, R.F. (1990) Studies on Cyanidium caldarium phycobiliprotein pigment mutants. Plant Physiol. 93: 772–777.PubMedCrossRefGoogle Scholar
  30. Logares, R., Rengefors, K., Kremp, A., Shalchian-Tabrizi, K., Boltovskoy, A., Tengs, T., Shurtleff, A. and Klaveness, D. (2007) Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution? Microb. Ecol. 53: 549–561.PubMedCrossRefGoogle Scholar
  31. Matsuzaki, M., Misumi, O., Shin-I, T., Maruyama, S., Takahara, M., Miyagishima, S.Y. and Mori, T. (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428: 653–657.PubMedCrossRefGoogle Scholar
  32. Miller, S.R., Purugganan, M.D. and Curtis, S.E. (2006) Molecular population genetics and phenotypic diversification of two populations of the thermophilic cyanobacterium Mastigocladus laminosus. Appl. Environ. Microbiol. 72: 2793–2800.PubMedCrossRefGoogle Scholar
  33. Nordstrom, D.K., Ball, J.W. and McClesey, R.B. (2005) Ground water to surface water: chemistry of thermal outflows in Yellowstone National Pak, In: W.P. Inskeep (ed.) Geothermal Biology and Geochemistry in Yellowstone National Park. Thermal Biology Institute, Montana, pp. 73–94.Google Scholar
  34. Oesterhelt, C. and Gross, W. (2002) Different sugar kinases are involved in the sugar sensing of Galdieria sulphuraria. Plant Physiol. 128: 291–299.PubMedCrossRefGoogle Scholar
  35. Ohta, N., Sato, N. and Kuroiwa, T. (1998) Structure and organization of the mitochondrial genome of the unicellular red algae Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res. 26: 5190–5198.PubMedCrossRefGoogle Scholar
  36. Ohta, N. et al. (2003) Complete sequence analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res. 10: 67–77.PubMedCrossRefGoogle Scholar
  37. Phelps, D. (1980) Distribution of soil mercury and the development of soil mercury anomalies in the Yellowstone geothermal area, Wyoming. Econ. Geol. 75: 730–741.CrossRefGoogle Scholar
  38. Pinto, G. and Taddei, R. (1986) Evaluation of toxic effects of heavy metals on unicellular algae. V – analysis of the inhibition manifesting itself with an increased lag phase. Boll. Soc. Natur. Napoli 95: 303–316.Google Scholar
  39. Pinto, G. (2007) Cyanidiophyceae: looking back – looking forward, In: J. Seckbach (ed.) Algae and Cyanobacteria in Extreme Environments. Springer, Dordrecht, The Netherlands, pp. 389–397.Google Scholar
  40. Pinto, G., Albertano, P. and Pollio, A. (1994) Italy’s contribution the the systematics of Cyanidiumn caldarium ‘sensu lato’, In: J. Seckbach (ed.) Evolutionary Pathways and Enigmatic Algae: Cyanidium caldarium (Rhodophyta) and Related Cells. Kluwer, Dordrecht, The Netherlands, pp. 157–166.CrossRefGoogle Scholar
  41. Planer-Friedrich, B. and Merkel, B.J. (2006) Volatile metals and metalloids in hydrothermal gases. Environ. Sci. Technol. 40: 3181–3187.PubMedCrossRefGoogle Scholar
  42. Planer-Friedrich, B., Lehr, C., Matschullat, J., Merkel, B.J., Nordstrom, D.K. and Sandstrom, M.W. (2006) Speciation of volatile arsenic at geothermal features in Yellowstone National Park. Geochimica 70: 2480–2491.CrossRefGoogle Scholar
  43. Proctor, V.W. (1959) Dispersal of fresh-water algae by migratory water birds. Science 130: 623–624.PubMedCrossRefGoogle Scholar
  44. Toplin, J.A., Norris, T.B., Lehr, C.R., McDermott, T.R. and Castenholz, R.W. (2008) The thermo-acidophilic Cyanidiales: biogeographic and phylogenetic diversity in Yellowstone National Park, Japan, and New Zealand. Appl. Environ. Microbiol. 74: 2822–2833.PubMedCrossRefGoogle Scholar
  45. Walker, J.J., Spear, J.R. and Pace, N. (2005) Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434: 1011–1014.PubMedCrossRefGoogle Scholar
  46. Ward, D.M. and Castenholz, R.W. (2000) Cyanobacteria in geothermal habitats, In: B.A. Whitton and M. Potts (eds.) Ecology of Cyanobacteria: Their Diversity in Time and Space. Kluwer, Dordrecht, The Netherlands, pp. 37–59.Google Scholar
  47. Ward, D.M., Bateson, M.M., Ferris, M.J., Kühl, M., Wieland, A., Koeppel, A. and Cohan, F.M. (2006) Cyanobacterial ecotypes in the microbial mat community of Mushroom Spring (Yellowstone National Park, Wyoming) as species-like units linking microbial community composition, structure and function. Philos. Trans. R. Society Lond. B. Biol. Sci. 361: 1997–2008.CrossRefGoogle Scholar
  48. Whitaker, R.J., Grogan, D.W. and Taylor, J.W. (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301: 976–978.PubMedCrossRefGoogle Scholar
  49. Yoon, S.Y., Hackett, J.D., Pinto, G. and Bhattacharya, D. (2002) The single, ancient origin of chromist plastids. Proc. Natl. Acad. Sci. USA 99: 15507–15512.PubMedCrossRefGoogle Scholar
  50. Yoon, S.Y., Hackett, J.D., Ciniglia, C., Pinto, G. and Bhattacharya, D. (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21: 809–818.PubMedCrossRefGoogle Scholar
  51. Yoon, H.S., Ciniglia, C., Wu, M., Comeron, J.M., Pinto, G., Pollio, A. and Bhattacharya, D. (2006a) Establishment of endolithic populations of extremeophilic Cyanidiales (Rhodophyta). BMC Evol. Biol. 6: 78 (12 pp) (online).PubMedCrossRefGoogle Scholar
  52. Yoon, H.S., Muller, K.M., Sheath, R.G., Ott, F.D. and Bhattacharya, D. (2006b) Defining the major lineages of red algae (Rhodophyta). J. Phycol. 42: 482–492.CrossRefGoogle Scholar
  53. Yoshimura, E., Nagasaka, S., Sato, Y., Satake, K. and Mori, S. (1999) Extraordinary high aluminum tolerance of the acidophilic thermophjilic alga, Cyanidium caldarium. Soil Sci. Plant Nutr. 45: 721–724.CrossRefGoogle Scholar
  54. Yoshimura, E., Nagasaka, S., Satake, K. and Mori, S. (2000) Mechanism of aluminum tolerance in Cyanidium caldarium. Hydrobiologia 433: 57–60.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Center for Ecology and Evolutionary BiologyUniversity of OregonEugeneUSA
  2. 2.Thermal Biology Institute and Department of Land ResourcesEnvironmental Sciences Montana State UniversityBozemanUSA

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