Abstract
Continental hydrothermal systems are a dynamic component of global thermal and geochemical cycles, exerting a pronounced impact on water chemistry and heat storage. As such, these environments are commonly classified by temperature, thermal fluid ionic concentration, and pH. Terrestrial hydrothermal systems are a refuge for extremophilic organisms, as extremes in temperature, metal concentration, and pH profoundly impact microorganism assemblage composition. While numerous studies focus on Bacteria and Archaea in these environments, few focus on Eukarya—likely due to lower temperature tolerances and because they are not model organisms for understanding the evolution of early life. However, where present, eukaryotic organisms are significant members of continental hydrothermal microorganism communities. Thus, this manuscript focuses on the eukaryotic occupants of terrestrial hydrothermal systems and provides a review of the current status of research, including microbe–eukaryote interactions and suggestions for future directions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilera Á (2013) Eukaryotic organisms in extreme acidic environments, the Río Tinto Case. Life 3:363–374. https://doi.org/10.3390/life3030363
Aguilera A, Souza-Egipsy V, Gómez F, Amils R (2007) Development and atructure of eukaryotic biofilms in an extreme acidic environment, Río Tinto (SW, Spain). Microb Ecol 53:294–305. https://doi.org/10.1007/s00248-006-9092-2
Aguilera Á, Souza-Egipsy V, González-Toril E et al (2010) Eukaryotic microbial diversity of phototrophic microbial mats in two Icelandic geothermal hot springs. Int Microbiol 13:21–32. https://doi.org/10.2436/20.1501.01.108
Amaral-Zettler LA (2013) Eukaryotic diversity at pH extremes. Front Microbiol 3:1–17. https://doi.org/10.3389/fmicb.2012.00441
Badirzadeh A, Niyyati M, Babaei Z et al (2011) Isolation of free-living amoebae from sarein hot springs in ardebil province, Iran. Iran J Parasitol 6:1–7
Baker BJ, Tyson GW, Goosherst L, Banfield JF (2009) Insights into the diversity of eukaryotes in acid mine drainage biofilm communities. Appl Environ Microbiol 75:2192–2199. https://doi.org/10.1128/AEM.02500-08
Baumgartner M, Yapi A, Gröbner-Ferreira R, Stetter KO (2003) Cultivation and properties of Echinamoeba thermarum n. sp., an extremely thermophilic amoeba thriving in hot springs. Extremophiles 7:267–274. https://doi.org/10.1007/s00792-003-0319-6
Baumgartner M, Eberhardt S, De Jonckheere JF, Stetter KO (2009) Tetramitus thermacidophilius nov. sp., an amoeboflagellate from acidic hot springs. J Eukaryot Microbiol 56:201–206
Blank CE, Cady SL, Pace NR (2002) Microbial composition of near-neutral silica-depositing thermal springs throughout Yellowstone National Park. Appl Environ Microbiol 1:703–718
Bodvarsson GS (1982) Mathematical modeling of the behavior of geothermal systems under exploitation. Dissertation, University of California-Berkeley
Bolhuis H, Cretoiu MS, Stal LJ (2014) Molecular ecology of microbial mats. Fed Eur Microbiol Soc Microb Ecol 90:335–350. https://doi.org/10.1111/1574-6941.12408
Bonny S, Jones B (2003) Relict tufa at Miette Hot Springs, Jasper National Park, Alberta, Canada. Can J Earth Sci 40:1459–1481. https://doi.org/10.1139/e03-050
Bottjer DJ (2005) Geobiology and the fossil record: eukaryotes, microbes, and their interactions. Palaeogeogr Palaeoclimatol Palaeoecol 219:5–21. https://doi.org/10.1016/j.palaeo.2004.10.011
Brock TD (1973) Lower pH limit for the existence of blue-green algae: evolutionary and ecological implications. Science (80-) 179:480–483
Brock TD (1978) Thermophilic microorganisms and life at high temperatures. Springer, New York
Brock TD, Boylen KL (1973) Presence of thermophilic bacteria in laundry and domestic hot-water heaters. Appl Microbiol 25:72–76
Brown PB, Wolfe GV (2006) Protist genetic diversity in the acidic hydrothermal environments of Lassen Volcanic National Park, USA. J Eukaryot Microbiol 53:420–431. https://doi.org/10.1111/j.1550-7408.2006.00125.x
Canganella F, Wiegel J (2011) Extremophiles: from abyssal to terrestrial ecosystems and possibly beyond. Naturwissenschaften 98:253–279. https://doi.org/10.1007/s00114-011-0775-2
Casamayor EO, Triadó-Margarit X, Castañeda C (2013) Microbial biodiversity in saline shallow lakes of the Monegros Desert, Spain. FEMS Microbiol Ecol 85:503–518. https://doi.org/10.1111/1574-6941.12139
Ciniglia C, Yoon HS, Pollio A et al (2004) Hidden biodiversity of the extremophilic Cyanidiales red algae. Mol Ecol 13:1827–1838. https://doi.org/10.1111/j.1365-294X.2004.02180.x
Cocquyt C (1999) Diatoms from a hot spring in Lake Tanganyika. Nov Hedwigia 68:425–439
Cohen AS (2003) Paleolimnology. Oxford University Press, Oxford
Costas E, Flores-Moya A, Perdigones N et al (2007) How eukaryotic algae can adapt to the Spain’s Rio Tinto: a neo-Darwinian proposal for rapid adaptation to an extremely hostile ecosystem. New Phytol 175:334–339. https://doi.org/10.1111/j.1469-8137.2007.02095.x
Cowan D, Tuffin M, Mulako I, Cass J (2012) Terrestrial Hydrothermal environments. In: Bell E (ed) Life at extremes: environments, organisms, and strategies for survival. CABI, Oxfordshire, pp 219–241
DeNicola DM (2000) A review of diatoms found in highly acidic environments. Hydrobiologia 433:111–122
Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev 2:95–108. https://doi.org/10.1038/nrmicro821
Hecky RE, Kilham P (1973) Diatoms in alkaline, saline lakes: ecology and geochemical implications. Limnol Oceanogr 18:53–71
Horikoshi K (2016) Extremophiles where it all began. Springer, Tokyo
Horikoshi K, Grant WD (eds) (1998) Extremophiles: microbial life in extreme environments. Wiley-Liss, New York
Horikoshi K, Antranikian G, Bull AT et al (2011) Extremophiles handbook. Springer, Tokyo
Idei M, Mayama S (2001) Pinnularia acidojaponica M. Idei et H. Kobayasi sp. nov. and P. valdetolerans Mayama et H. Kobayasi sp. nov.—new diatom taxa from Japanese extreme environments. In: Jahn R, Kociolek JP, Witkowski A, Compere P (eds) Lange–Bertalot–Festschrift. Gantner, Ruggell, pp 265–277
Jones B, Renaut RW, Rosen MR (1997) Biogenicity of silica precipitation around geysers and hot-spring vents, North Island, New Zealand. J Sediment Res 67:88–104
Kao PM, Hsu BM, Chen NH et al (2012) Isolation and identification of Acanthamoeba species from thermal spring environments in southern Taiwan. Exp Parasitol 130:354–358. https://doi.org/10.1016/j.exppara.2012.02.008
Kearns RA, Gesler WM (1998) Putting health into place: landscape, identity, and well-being. Syracuse University Press, New York
Kroll RG (1990) Alkalophiles. In: Edwards C (ed) Microbiology of extreme environments. McGraw-Hill, New York, pp 55–92
LaPaglia C, Hartzell PL (1997) Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 63:3158–3163
López-Rodas V, Marvá F, Rouco M et al (2008) Adaptation of the chlorophycean Dictyosphaerium chlorelloides to stressful acidic, mine metal-rich waters as result of pre-selective mutations. Chemosphere 72:703–707. https://doi.org/10.1016/j.chemosphere.2008.04.009
Lowell RP (1991) Continental systems and submarine hydrothermal. Geophysics 29:457–476
Lynn R, Brock TD (1969) Notes on the ecology of a species of Zygogonium (Kütz.) in Yellowstone National Park. J Phycol 5:181–185
MacElroy RD (1974) Some comments on the evolution of extremophiles. Biosystems 6:74–75
Meadow JF, Zabinski CA (2012) Spatial heterogeneity of eukaryotic microbial communities in an unstudied geothermal diatomaceous biological soil crust: yellowstone National Park, WY, USA. Fed Eur Microbiol Soc Microb Ecol 82:182–191. https://doi.org/10.1111/j.1574-6941.2012.01416.x
Mpawenayo B, Mathooko JM (2004) Diatom assemblages in the hotsprings associated with Lakes Elmenteita and Baringo in Kenya. Afr J Ecol 42:363–367. https://doi.org/10.1111/j.1365-2028.1997.100-89100.x
Niyyati M, Latifi A (2017) Free living Amoeba belonging to Vannella spp. isolated from a hotspring in Amol City, Northern Iran. Novelty in Biomedicine 2:85–88
Nozaki H, Takano H, Misumi O et al (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28. https://doi.org/10.1186/1741-7007-5-28
Owen RB, Renaut RW, Jones B (2008) Geothermal diatoms: a comparative study of floras in hot spring systems of Iceland, New Zealand, and Kenya. Hydrobiologia 610:175–192. https://doi.org/10.1007/s10750-008-9432-y
Pan WZ, Huang XW, Wei KB et al (2010) Diversity of thermophilic fungi in Tengchong Rehai national park revealed by ITS nucleotide sequence analyses. J Microbiol 48:146–152. https://doi.org/10.1007/s12275-010-9157-2
Prieto-Barajas CM, Valencia-Cantero E, Santoyo G (2017) Microbial mat ecosystems: structure types, functional diversity, and biotechnological application. Electron J Biotechnol 31:48–56. https://doi.org/10.1016/j.ejbt.2017.11.001
Pumas C, Pruetiworanan S, Peerapornpisal Y (2018) Diatom diversity in some hot springs of northern Thailand. Botanica 24:69–86. https://doi.org/10.2478/botlit-2018-0007
Qin J, Lehr CR, Yuan C et al (2009) Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci 106:5213–5217
Rampelotto PH (2013) Extremophiles and extreme environments. Life 3:482–485. https://doi.org/10.3390/life3030482
Redman RS, Litvintseva A, Sheehan KB et al (1999) Fungi from geothermal soils in Yellowstone National Park. Appl Environ Microbiol 65:5193–5197
Riding R (2000) Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47:179–214. https://doi.org/10.1046/j.1365-3091.2000.00003.x
Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101. https://doi.org/10.1038/35059215
Schleper C, Puehler G, Holz I et al (1995) Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177:7050–7059
Schonknecht G, Chen W-H, Ternes CM et al (2013) Gene transfer from Bacteria and Archaea facilitated evolution of an extremophilic eukaryote. Science (80-) 339:1207–1210. https://doi.org/10.1126/science.1231707
Seckbach J (ed) (1994) Evolutionary pathways and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells. Springer Science, Dordrecht
Seckbach J (ed) (2007) Algae and cyanobacteria in extreme environments. Springer, Dordrecht
Seilacher A (1999) Biomat-related life styles in the Precambrian. Palaios 14:86–93
Selvarajan R, Sibanda T, Tekere M (2018) Thermophilic bacterial communities inhabiting the microbial mats of “indifferent” and chalybeate (iron-rich) thermal springs: diversity and biotechnological analysis. Microbiologyopen 7:1–12. https://doi.org/10.1002/mbo3.560
Shanks WC, Alt JC, Morgan LA (2007) Geochemistry of sublacustrine hydrothermal deposits in Yellowstone Lake-hydrothermal reactions, stable-isotope systematics, sinter deposition, and spire formation. US Geol Surv Prof Pap 1717:205–234
Sheehan KB, Fagg JA, Ferris MJ, Henson JM (2003) Thermophilic Amoebae and legionella in hot springs in Yellowstone and Grand Teton National Parks. In: Geotherm Biololgy and Geochemistry in Yellowstone National Park. Montana State University Publications, Boseman, pp 317–324
Simpson AGB, Slamovits CH, Archibald JM (2017) Protist diversity and eukaryote phylogeny. In: Archibald JM, Simpson AGB, Slamovits CH (eds) Handbook of the protists. Springer, Heidelberg, pp 1–21
Singh S, Madlala AM, Prior BA (2003) Thermomyces lanuginosus: properties of strains and their hemicellulases. FEMS Microbiol Rev 27:3–16. https://doi.org/10.1016/S0168-6445(03)00018-4
Sittenfeld A, Mora M, Ortega JM et al (2002) Characterization of a photosynthetic Euglena strain isolated from an acidic hot mud pool of a volcanic area of Costa Rica. FEMS Microbiol Ecol 42:151–161. https://doi.org/10.1016/S0168-6496(02)00327-6
Sittenfeld A, Vargas M, Sánchez E et al (2004) Una nueva especie de Euglena (Euglenozoa: euglenales) aislada de ambientes extremófilos en las Pailas de Barro del Volcán Rincón de la Vieja, Costa Rica. Rev Biol Trop 52:27–30
Smol JP, Battarbee RW, Davis RB, Merilainen J (eds) (1986) Diatoms and lake acidity. Springer, Netherlands, Dordrecht
Stetter KO (1999) Extremophiles and their adaptation to hot environments. FEBS Lett 452:22–25. https://doi.org/10.1016/S0014-5793(99)00663-8
Stockner JG (1967) Observations of thermophilic algal communities in Mount Rainier and Yellowstone National Parks. Limnol Oceanogr 12:13–17
Tansey MR, Brock TD (1972) The upper temperature limit for eukaryotic organisms. Proc Natl Acad Sci USA 69:2426–2428
Tansey MR, Brock TD (1978) Microbial life at high temperatures: ecological aspects. In: Kushner DJ (ed) Microbial life in extreme environments. Academic, London, pp 159–216
Tekere M, Lötter A, Olivier J, Venter S (2015) Bacterial diversity in some South African thermal springs: a metagenomic analysis. In: Proceedings World Geothermal Congress. Melbourne, Australia, pp 19–25
Teske A (2007) Enigmatic archaeal and eukaryotic life at hydrothermal vents and in marine subsurface sediments. In: Seckback J (ed) Algae and cyanobacteria in extreme environments. Springer, Dordrecht, pp 519–533
Van de Vijver B, Cocquyt C (2009) Four new diatom species from La Calera hot spring in the Peruvian Andes (Colca Canyon). Diatom Res 24:209–223. https://doi.org/10.1080/0269249X.2009.9705792
Weber APM, Horst RJ, Barbier GG, Oesterhelt C (2007) Metabolism and metabolomics of eukaryotes living under extreme conditions. Int Rev Cytol 256:1–34. https://doi.org/10.1016/S0074-7696(07)56001-8
Wehr JD, Sheath RG (2003) Freshwater algae of North America. Academic, Amsterdam
Wiegel J, Adams MWW (eds) (1998) Thermophiles: the keys to the molecular evolution and the origin of life?. Taylor and Francis, London
Wilson M, Siering P, White C et al (2008) Novel archaea and bacteria dominate stable microbial communities in North America’s largest hot spring. Microb Ecol 56:292–305
Winsborough BM, Golubic S (1987) The role of diatoms in stromatolite growth: two examples from modern freshwater settings. J Phycol 23:195–201
Yamazaki A, Toyama K, Nakagiri A (2010) A new acidophilic fungus Teratosphaeria acidotherma (Capnodiales, Ascomycota) from a hot spring. Mycoscience 51:443–455. https://doi.org/10.1007/S10267-010-0059-2
Zhu T, Dittrich M (2016) Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology : a review. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2016.00004
Zirnstein I, Arnold T, Krawczyk-Bärsch E et al (2012) Eukaryotic life in biofilms formed in a uranium mine. Microbiologyopen 1:83–94. https://doi.org/10.1002/mbo3.17
Acknowledgements
The authors thank the anonymous reviewer for providing valuable feedback for improving the breadth of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by S. Albers.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Brown, S.R., Fritz, S.C. Eukaryotic organisms of continental hydrothermal systems. Extremophiles 23, 367–376 (2019). https://doi.org/10.1007/s00792-019-01101-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-019-01101-y