Eukaryotic organisms of continental hydrothermal systems
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.
Keywords
Eukaryotes Thermophiles Acidophiles Alkaliphiles GeothermalNotes
Acknowledgements
The authors thank the anonymous reviewer for providing valuable feedback for improving the breadth of this manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
References
- Aguilera Á (2013) Eukaryotic organisms in extreme acidic environments, the Río Tinto Case. Life 3:363–374. https://doi.org/10.3390/life3030363 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Amaral-Zettler LA (2013) Eukaryotic diversity at pH extremes. Front Microbiol 3:1–17. https://doi.org/10.3389/fmicb.2012.00441 CrossRefGoogle Scholar
- 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 6:1–7PubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Baumgartner M, Eberhardt S, De Jonckheere JF, Stetter KO (2009) Tetramitus thermacidophilius nov. sp., an amoeboflagellate from acidic hot springs. J Eukaryot Microbiol 56:201–206PubMedCrossRefGoogle Scholar
- Blank CE, Cady SL, Pace NR (2002) Microbial composition of near-neutral silica-depositing thermal springs throughout Yellowstone National Park. Appl Environ Microbiol 1:703–718Google Scholar
- Bodvarsson GS (1982) Mathematical modeling of the behavior of geothermal systems under exploitation. Dissertation, University of California-BerkeleyGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Brock TD (1973) Lower pH limit for the existence of blue-green algae: evolutionary and ecological implications. Science (80-) 179:480–483CrossRefGoogle Scholar
- Brock TD (1978) Thermophilic microorganisms and life at high temperatures. Springer, New YorkCrossRefGoogle Scholar
- Brock TD, Boylen KL (1973) Presence of thermophilic bacteria in laundry and domestic hot-water heaters. Appl Microbiol 25:72–76PubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- Cocquyt C (1999) Diatoms from a hot spring in Lake Tanganyika. Nov Hedwigia 68:425–439Google Scholar
- Cohen AS (2003) Paleolimnology. Oxford University Press, OxfordGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 219–241CrossRefGoogle Scholar
- DeNicola DM (2000) A review of diatoms found in highly acidic environments. Hydrobiologia 433:111–122CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Hecky RE, Kilham P (1973) Diatoms in alkaline, saline lakes: ecology and geochemical implications. Limnol Oceanogr 18:53–71CrossRefGoogle Scholar
- Horikoshi K (2016) Extremophiles where it all began. Springer, TokyoGoogle Scholar
- Horikoshi K, Grant WD (eds) (1998) Extremophiles: microbial life in extreme environments. Wiley-Liss, New YorkGoogle Scholar
- Horikoshi K, Antranikian G, Bull AT et al (2011) Extremophiles handbook. Springer, TokyoCrossRefGoogle Scholar
- 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 265–277Google Scholar
- Jones B, Renaut RW, Rosen MR (1997) Biogenicity of silica precipitation around geysers and hot-spring vents, North Island, New Zealand. J Sediment Res 67:88–104Google Scholar
- 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 CrossRefPubMedGoogle Scholar
- Kearns RA, Gesler WM (1998) Putting health into place: landscape, identity, and well-being. Syracuse University Press, New YorkGoogle Scholar
- Kroll RG (1990) Alkalophiles. In: Edwards C (ed) Microbiology of extreme environments. McGraw-Hill, New York, pp 55–92Google Scholar
- LaPaglia C, Hartzell PL (1997) Stress-induced production of biofilm in the hyperthermophile Archaeoglobus fulgidus. Appl Environ Microbiol 63:3158–3163PubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- Lowell RP (1991) Continental systems and submarine hydrothermal. Geophysics 29:457–476CrossRefGoogle Scholar
- Lynn R, Brock TD (1969) Notes on the ecology of a species of Zygogonium (Kütz.) in Yellowstone National Park. J Phycol 5:181–185PubMedCrossRefPubMedCentralGoogle Scholar
- MacElroy RD (1974) Some comments on the evolution of extremophiles. Biosystems 6:74–75CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Niyyati M, Latifi A (2017) Free living Amoeba belonging to Vannella spp. isolated from a hotspring in Amol City, Northern Iran. Novelty in Biomedicine 2:85–88Google Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Qin J, Lehr CR, Yuan C et al (2009) Biotransformation of arsenic by a Yellowstone thermoacidophilic eukaryotic alga. Proc Natl Acad Sci 106:5213–5217PubMedCrossRefGoogle Scholar
- Rampelotto PH (2013) Extremophiles and extreme environments. Life 3:482–485. https://doi.org/10.3390/life3030482 CrossRefPubMedPubMedCentralGoogle Scholar
- Redman RS, Litvintseva A, Sheehan KB et al (1999) Fungi from geothermal soils in Yellowstone National Park. Appl Environ Microbiol 65:5193–5197PubMedPubMedCentralGoogle Scholar
- 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 CrossRefGoogle Scholar
- Rothschild LJ, Mancinelli RL (2001) Life in extreme environments. Nature 409:1092–1101. https://doi.org/10.1038/35059215 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 177:7050–7059PubMedPubMedCentralCrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- Seckbach J (ed) (1994) Evolutionary pathways and enigmatic algae: Cyanidium caldarium (Rhodophyta) and related cells. Springer Science, DordrechtGoogle Scholar
- Seckbach J (ed) (2007) Algae and cyanobacteria in extreme environments. Springer, DordrechtGoogle Scholar
- Seilacher A (1999) Biomat-related life styles in the Precambrian. Palaios 14:86–93CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 1717:205–234Google Scholar
- 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 317–324Google Scholar
- 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 1–21Google Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 52:27–30PubMedCrossRefPubMedCentralGoogle Scholar
- Smol JP, Battarbee RW, Davis RB, Merilainen J (eds) (1986) Diatoms and lake acidity. Springer, Netherlands, DordrechtGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- Stockner JG (1967) Observations of thermophilic algal communities in Mount Rainier and Yellowstone National Parks. Limnol Oceanogr 12:13–17CrossRefGoogle Scholar
- Tansey MR, Brock TD (1972) The upper temperature limit for eukaryotic organisms. Proc Natl Acad Sci USA 69:2426–2428PubMedCrossRefPubMedCentralGoogle Scholar
- Tansey MR, Brock TD (1978) Microbial life at high temperatures: ecological aspects. In: Kushner DJ (ed) Microbial life in extreme environments. Academic, London, pp 159–216Google Scholar
- 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 19–25Google Scholar
- 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 519–533CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedGoogle Scholar
- Wehr JD, Sheath RG (2003) Freshwater algae of North America. Academic, AmsterdamGoogle Scholar
- Wiegel J, Adams MWW (eds) (1998) Thermophiles: the keys to the molecular evolution and the origin of life?. Taylor and Francis, LondonGoogle Scholar
- 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 56:292–305PubMedCrossRefGoogle Scholar
- Winsborough BM, Golubic S (1987) The role of diatoms in stromatolite growth: two examples from modern freshwater settings. J Phycol 23:195–201CrossRefGoogle Scholar
- 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 CrossRefGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar
- 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 CrossRefPubMedPubMedCentralGoogle Scholar