Cyanidiales: Evolution and Habitats

  • Shinya MiyagishimaEmail author
  • Jong Lin Wei
  • Hisayoshi Nozaki
  • Shunsuke Hirooka


Cyanidioschyzon merolae is a unicellular alga without a cell wall that inhabits sulfuric hot springs. It is a member of the red algae Cyanidiales that diverged from other red algal lineages approximately 1.3–1.4 billion years ago. Cyanidiales are the only eukaryotes and phototrophic organisms found in sulfuric hot springs, but some rare species have also been found in nonthermal and/or neutrophilic environments. They are classified into three genera, namely, Galdieria, Cyanidium, and Cyanidioschyzon. Galdieria can grow heterotrophically and mixotrophically in contrast to the (almost) obligate photoautotrophs Cyanidium and Cyanidioschyzon. Cells of Galdieria and Cyanidium are surrounded by a rigid cell wall and proliferate by forming autospores in the mother cell wall. In contrast, Cyanidioschyzon lacks a cell wall and proliferates by binary fission. Recent phylogenetic studies have classified Cyanidiales into four distinct lineages: Galdieria lineage, acidophilic Cyanidium lineage, neutrophilic Cyanidium lineage, and the lineage that comprises G. maxima, Galdieria-like algae, and Cyanidioschyzon. Recent studies using high-throughput sequencing technologies have started to reveal that both gene losses and horizontal gene transfer from environmental prokaryotes have contributed to the emergence and diversification of Cyanidiales and their adaptation to respective habitats.


Acidophile Cyanidiale Cyanidiophyceae Cyanidioschyzon Galdieria Cyanidium 



We thank Dr. Sumiya (Keio University) for helping us to take photographs of Cyanidiales in their natural habitats. Our study was partly supported by Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research 25251039 (to S.M.) and by the Core Research for Evolutional Science and Technology Program of the Japan Science and Technology Agency (S.M.).


  1. Adl SM, Simpson AG, Lane CE, Lukes J et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–493CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aguilera A, Souza-Egipsy V et al (2007) Development and structure of eukaryotic biofilms in an extreme acidic environment, rio tinto (SW, Spain). Microb Ecol 53:294–305CrossRefPubMedGoogle Scholar
  3. Albertano P, Pinto G (1986) The action of heavy metals on the growth of the acidophilic algae. Boll Soc Nat Napoli 45:319–328Google Scholar
  4. Albertano P, Ciniglia C et al (2000) The taxonomic position of Cyanidium, Cyanidioschyzon and Galdieria: an update. Hydrobiologia 433:137–143CrossRefGoogle Scholar
  5. Baker BJ, Lutz MA et al (2004) Metabolically active eukaryotic communities in extremely acidic mine drainage. Appl Environ Microbiol 70:6264–6271CrossRefPubMedPubMedCentralGoogle Scholar
  6. Castenholz RW, McDermott TR (2010) The cyanidiales: ecology, biodiversity, and biogeography. In: Seckbach J, Chapman DJ (eds) Red algae in the genomic age. Springer, Drodrecht, pp 359–371Google Scholar
  7. Ciniglia C, Yoon HS et al (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol Ecol 13:1827–1838CrossRefPubMedGoogle Scholar
  8. Ciniglia C, Yang EC et al (2014) Cyanidiophyceae in Iceland: plastid rbcL gene elucidates origin and dispersal of extremophilic Galdieria sulphuraria and G. maxima (Galdieriaceae, Rhodophyta). Phycologia 53:542–551CrossRefGoogle Scholar
  9. De Luca P, Taddei R (1970) Due alghe delle fumarole acide dei Campi Flegrei (Napoli): Cyanidium caldarium? Delpinoa 10/11:79–89Google Scholar
  10. De Luca P, Taddei R et al (1978) “Cyanidioschyzon merolae”: a new alga of thermal acidic environments. Webbia 33:37–44CrossRefGoogle Scholar
  11. Doemel WN, Brock TD (1971) The physiological ecology of Cyunidium caldarium. J Gen Microbiol 67:17–32CrossRefGoogle Scholar
  12. Elias M, Archibald JM (2009) Sizing up the genomic footprint of endosymbiosis. BioEssays 31:1273–1279CrossRefPubMedGoogle Scholar
  13. Ferris MJ, Sheehan KB et al (2005) Algal species and light microenvironment in a low-pH, geothermal microbial mat community. Appl Environ Microbiol 71:7164–7171CrossRefPubMedPubMedCentralGoogle Scholar
  14. Friedmann I (1964) Progress in the biological exploration of caves and subterranean waters in Israel. Int J Speleol 1:29–33CrossRefGoogle Scholar
  15. Geitler L (1933) Diagnoses neuer Blaualgen von den Sunda-Insela. Arch Hydrobiol Suppl 12:622–634Google Scholar
  16. Graham LD, Wilcox LW (2000) Algae. Prentice Hall, Upper Saddle RiverGoogle Scholar
  17. Gross W (1999) Revision of comparative traits for the acido- and thermophilic red algae Cyanidium and Galdieria. In: Seckbach J (ed) Evolutionary pathways and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells. Springer, Dordrecht, pp 437–446Google Scholar
  18. Gross W (2000) Ecophysiology of algae living in highly acidic environments. Hydrobiologia 33:31–37CrossRefGoogle Scholar
  19. Gross W, Gross S (2001) Physiological characterization of the red alga Galdieria sulphuraria isolated from a mining area. Nova Hedwigia Beih 123:523–530Google Scholar
  20. Gross W, Schnarrenberger C (1995) Heterotrophic growth of 2 strains of the acido-thermophilic red alga Galdieria sulphuraria. Plant Cell Physiol 36:633–638Google Scholar
  21. Gross W, Oesterhelt C et al (2002) Characterization of a non-thermophilic strain of the red algal genus Galdieria isolated from Soos (Czech Republic). Eur J Phycol 37:477–482CrossRefGoogle Scholar
  22. Hirose H (1950) Studies of thermal alga, Cyanidium caldarium. Bot Mag Tokyo 63:745–746CrossRefGoogle Scholar
  23. Hoffman L (1994) Cyanidium-like algae from caves. In: Seckbach J (ed) Evolutionary pathways and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells. Kluwer, Dordrecht, pp 175–182CrossRefGoogle Scholar
  24. Leclerc JC, Coute A et al (1983) Le climat annuel de deux grottes et d’une église du Poitou, ou vivent des colonies pures d’algues sciaphiles. Algol 4:1–19Google Scholar
  25. Lin S, Offner GD et al (1990) Studies on Cyanidium caldarium phycobiliprotein pigment mutants. Plant Physiol 93:772–777CrossRefPubMedPubMedCentralGoogle Scholar
  26. Matsuzaki M, Misumi O et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657CrossRefPubMedGoogle Scholar
  27. Meneghini G (1839) Nuova specie di alga descritta dal Sig. Dott. Giuseppe Meneghini di Padova. Nuovo Giorn Lett Sci 39:67–68Google Scholar
  28. Merola A, Castaldo R et al (1981) Revision of Cyanidium caldarium: three species of acidophilic algae. Gio Bot Ital 115:189–195CrossRefGoogle Scholar
  29. Minoda A, Sakagami R et al (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45:667–671CrossRefPubMedGoogle Scholar
  30. Moreira D, López-Archilla A et al (1994) Characterization of two new thermoacidophilic microalgae: genome organization and comparison with Galdieria sulphuraria. FEMS Lett 122:109–114CrossRefGoogle Scholar
  31. Moriyama T, Mori N et al (2015) Activation of oxidative carbon metabolism by nutritional enrichment by photosynthesis and exogenous organic compounds in the red alga Cyanidioschyzon merolae: evidence for heterotrophic growth. Springerplus 4:559CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nagasaka S, Nishizawa NK et al (2004) Metal metabolism in the red alga Cyanidium caldarium and its relationship to metal tolerance. Biometals 17:177–181CrossRefPubMedGoogle Scholar
  33. Novis P, Harding JS (2007) Extreme acidophiles: freshwater algae associated with acid mine drainage. Algae and cyanobacteria in extreme environments. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 443–463Google Scholar
  34. Nozaki H, Takano H et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28CrossRefPubMedPubMedCentralGoogle Scholar
  35. Oesterhelt C, Schnarrenberger C et al (1999) Characterization of a sugar/polyol uptake system in the red alga Galdieria sulphuraria. Eur J Phycol 34:271–277CrossRefGoogle Scholar
  36. Ohnuma M, Yokoyama T et al (2008) Polyethylene glycol (PEG)-mediated transient gene expression in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 49:117–120CrossRefPubMedGoogle Scholar
  37. Ohnuma M, Misumi O et al (2011) Phototaxis in the unicellular red algae Cyanidioschyzon merolae and Cyanidium caldarium. Cytologia 76:295–300CrossRefGoogle Scholar
  38. Ohta N, Sato N et al (1998) Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res 26:5190–5198CrossRefPubMedPubMedCentralGoogle Scholar
  39. Ohta N, Matsuzaki M et al (2003) Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 10:67–77CrossRefPubMedGoogle Scholar
  40. Okuwaki T, Takahashi H et al (1996) Ultrastructures of the Golgi body and cell surface in Cyanidioschyzon merolae. Cytologia 61:69–74CrossRefGoogle Scholar
  41. Pinto G (2007) Cyanidiophyceae: looking back–looking forward. In: Seckbach J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 387–397CrossRefGoogle Scholar
  42. Pinto G, Taddei R (1978) Le alghe delle acque e dei suoli acidi italiani. Delpinoa 18(19):77–106Google Scholar
  43. Qiu H, Price DC et al (2013) Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea. Curr Biol 23:R865–R866CrossRefPubMedGoogle Scholar
  44. Reeb V, Bhattacharya D (2010) The thermo-acidophilic Cyanidiophyceae (Cyanidiales). In: Seckbach J, Chapman DJ (eds) Red algae in the genomic age. Springer, Dordrecht, pp 411–426Google Scholar
  45. Rigano C, Fuggi A et al (1976) Studies on utilization of 2-ketoglutarate, glutamate and other amino acids by the unicellular alga Cyanidium caldarium. Arch Microbiol 107:133–138CrossRefPubMedGoogle Scholar
  46. Rigano C, Aliotta G et al (1977) Heterotrophic growth patterns in the unicellular alga Cyanidium caldarium. A possible role for threonine dehydrase. Arch Microbiol 113:191–196CrossRefPubMedGoogle Scholar
  47. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  48. Schonknecht G, Chen WH et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210CrossRefPubMedGoogle Scholar
  49. Schwabe GH (1936) Über einige Blaualgen aus dem mittleren und sudlichen Chile. Verh des Deutsch Wiss Ver Santiago de Chile 3:113–174Google Scholar
  50. Sentsova OY (1994) The study of Cyanidiophyceae in Russia. Algae of genus Galdieria: diversity, characterization and occurrence in mixed populations with Cyanidium caldarium. In: Seckbach J (ed) Evolutionary pathways and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells. Springer, Dordrecht, pp 167–174CrossRefGoogle Scholar
  51. Skorupa DJ, Reeb V et al (2013) Cyanidiales diversity in Yellowstone national park. Lett Appl Microbiol 57:459–466CrossRefPubMedGoogle Scholar
  52. Skuja H (1970) Alghe cavernicole nelle zone illuminate delle Grotte di Castellana (Murge di Bari). Le Grotte d’Italia 4:193–202Google Scholar
  53. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  54. Toplin JA, Norris TB et al (2008) Biogeographic and phylogenetic diversity of thermoacidophilic cyanidiales in Yellowstone National Park, Japan, and New Zealand. Appl Environ Microbiol 74:2822–2833CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ward DM, Castenholz RW (2000) Cyanobacteria in geothermal habitats. In: Whitton BA, Potts M (eds) Ecology of cyanobacteria: their diversity in time and space. Kluwer, Dordrecht, pp 37–59Google Scholar
  56. Yagisawa F, Nishida K et al (2007) Identification and mitotic partitioning strategies of vacuoles in the unicellular red alga Cyanidioschyzon merolae. Planta 226:1017–1029CrossRefPubMedGoogle Scholar
  57. Yagisawa F, Fujiwara T et al (2013) Golgi inheritance in the primitive red alga, Cyanidioschyzon merolae. Protoplasma 250:943–948CrossRefPubMedGoogle Scholar
  58. Yoon HS, Hackett JD et al (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818CrossRefPubMedGoogle Scholar
  59. Yoon HS, Ciniglia C et al (2006a) Establishment of endolithic populations of extremophilic Cyanidiales (Rhodophyta). BMC Evol Biol 6:78CrossRefPubMedPubMedCentralGoogle Scholar
  60. Yoon HS, Müller KM et al (2006b) Defining the major lineages of red algae (Rhodophyta). J Phycol 42:482–492CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Shinya Miyagishima
    • 1
    Email author
  • Jong Lin Wei
    • 1
    • 3
  • Hisayoshi Nozaki
    • 4
  • Shunsuke Hirooka
    • 1
    • 2
  1. 1.Department of Cell GeneticsNational Institute of GeneticsShizuokaJapan
  2. 2.Core Research for Evolutional Science and Technology ProgramJapan Science and Technology AgencySaitamaJapan
  3. 3.Department of GeneticsGraduate University for Advanced StudiesShizuokaJapan
  4. 4.Department of Biological Sciences, Graduate School of ScienceUniversity of TokyoTokyoJapan

Personalised recommendations