Article | Published:

The ecology and diversity of microbial eukaryotes in geothermal springs

The ISME Journalvolume 12pages19181928 (2018) | Download Citation

Abstract

Decades of research into the Bacteria and Archaea living in geothermal spring ecosystems have yielded great insight into the diversity of life and organismal adaptations to extreme environmental conditions. Surprisingly, while microbial eukaryotes (protists) are also ubiquitous in many environments, their diversity across geothermal springs has mostly been ignored. We used high-throughput sequencing to illuminate the diversity and structure of microbial eukaryotic communities found in 160 geothermal springs with broad ranges in temperature and pH across the Taupō Volcanic Zone in New Zealand. Protistan communities were moderately predictable in composition and varied most strongly across gradients in pH and temperature. Moreover, this variation mirrored patterns observed for bacterial and archaeal communities across the same spring samples, highlighting that there are similar ecological constraints across the tree of life. While extreme pH values were associated with declining protist diversity, high temperature springs harbored substantial amounts of protist diversity. Although protists are often overlooked in geothermal springs and other extreme environments, our results indicate that such environments can host distinct and diverse protistan communities.

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References

  1. 1.

    Pace NR. A molecular view of microbial diversity and the biosphere. Science. 1997;276:734–40.

  2. 2.

    Hugenholtz P, Pitulle C, Hershberger KL, Pace NR. Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol. 1998;180:366–76.

  3. 3.

    Rothschild LJ, Mancinelli RL. Life in extreme environments. Nature. 2001;409:1092–101.

  4. 4.

    Lowe SE, Jain MK, Zeikus JG. Biology ecology and biotechnological applications of anaerobic bacteria adapted to environmental stresses in temperature pH salinity or substrates. Microbiol Rev. 1993;57:451–509.

  5. 5.

    Ferrer M, Golyshina O, Beloqui A, Golyshin PN. Mining enzymes from extreme environments. Curr Opin Microbiol. 2007;10:207–14.

  6. 6.

    Goh KM, Kahar UM, Chai YY, Chong CS, Chai KP, Ranjani V, et al. Recent discoveries and applications of Anoxybacillus. Appl Microbiol Biotechnol. 2013;97:1475–88.

  7. 7.

    Chien A, Edgar DB, Trela JM. Deoxyribonucleic acid polymerase from the extreme thermophile Thermus aquaticus. J Bacteriol. 1976;127:1550–7.

  8. 8.

    Brock TD, Freeze H. Thermus aquaticus gen nov. and sp. nov. a nonsporulating extreme thermophile. J Bacteriol. 1969;98:289–97.

  9. 9.

    Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, Thomas WK. Sequencing our way towards understanding global eukaryotic biodiversity. Trends Ecol Evolut. 2012;27:233–43.

  10. 10.

    Brock TD. Lower pH limit for the existence of blue-green algae: evolutionary and ecological implications. Science. 1973;179:480–3.

  11. 11.

    Brown PB, Wolfe GV. Protist genetic diversity in the acidic hydrothermal environments of Lassen Volcanic National Park USA. J Euk Microbiol. 2006;53:420–31.

  12. 12.

    Baumgartner M, Yapi A, Gröbner-Ferreira R, Stetter KO. Cultivation and properties of Echinamoeba thermarum nov. sp., an extremely thermophilic amoeba thriving in hot springs. Extremophiles. 2003;7:267–74.

  13. 13.

    Ramaley RF, Scanlan PL, O’Dell WD. Presence of thermophilic Naegleria isolates in the Yellowstone and Grand Teton national parks. Thermophiles Biodiversity, Ecology, and Evolution. US: Springer; 2001. p. 41–50.

  14. 14.

    Amaral-Zettler LA, Gomez F, Zettler E, Keenan BG, Amils R, Sogin M. Microbiology: eukaryotic diversity in Spain’s River of Fire. Nature. 2002;417:137–137.

  15. 15.

    Amaral-Zettler LA. Eukaryotic diversity at pH extremes. Front Microbiol. 2013;3:441.

  16. 16.

    Brock TD. The genus Cyanidium. Thermophilic microorganisms and life at high temperatures. New York: Springer; 1978; p. 255–302.

  17. 17.

    Sittenfeld A, Mora M, Oretega JM, Albertazzi F, Cordero A, Roncel M, et al. Characterization of a photosynthetic Euglena strain isolated from an acidic hot mud pool of a volcanic area of Costa Rica. FEMS Microbiol Ecol. 2002;42:151–61.

  18. 18.

    Aguilera Á, Souza-Egipsy V, González-Toril E, Rendueles O, Amils R. Eukaryotic microbial diversity of phototrophic microbial mats in two Icelandic geothermal hot springs. Int Microbiol. 2010;13:21–32.

  19. 19.

    Levinsen H, Turner JT, Nielsen TG, Hansen BW. On the trophic coupling between protists and copepods in arctic marine ecosystems. Mar Ecol Prog Ser. 2000;204:65–77.

  20. 20.

    Wardle DA. The influence of biotic interactions on soil biodiversity. Ecol Lett. 2006;9:870–86.

  21. 21.

    Geisen S, Laros I, Vizcaíno A, Bonkowski M, de Groot GA. Not all are free‐living: high‐throughput DNA metabarcoding reveals a diverse community of protists parasitizing soil metazoan. Mol Ecol. 2015;24:4556–69.

  22. 22.

    Reeder WH, Sanck J, Hirst M, Dawson SC, Wolfe GV. The Food Web of Boiling Springs Lake Appears Dominated by the Heterolobosean Tetramitus thermacidophilus Strain BSL. J Euk Microbiol. 2015;62:374–90.

  23. 23.

    Sharp CE, Brady AL, Sharp GH, Grasby SE, Stott MB, Dunfield PF. Humboldt’s spa: microbial diversity is controlled by temperature in geothermal environments. ISME J. 2014;8:1166–74.

  24. 24.

    Chiriac CM, Szekeres E, Rudi K, Baricz A, Hegedus A, Dragoş N, et al. Differences in temperature and water chemistry shape distinct diversity patterns in thermophilic microbial communities. Appl Environ Microbiol. 2017;83:e01363–17.

  25. 25.

    Oliverio AM, Bradford MA, Fierer N. Identifying the microbial taxa that consistently respond to soil warming across time and space. Glob Change Biol. 2017;23:2117–29.

  26. 26.

    Ramirez KS, Leff JW, Barberan A, Bates ST, Betley J, Crowther T, et al. Biogeographic patterns in below-ground diversity in New York City’s Central Park are similar to those observed globally. Proc R Soc B. 2014;281:20141988.

  27. 27.

    Dupont AÖC, Griffiths RI, Bell T, Bass D. Differences in soil micro‐eukaryotic communities over soil pH gradients are strongly driven by parasites and saprotrophs. Env Microbiol. 2016;18:2010–24.

  28. 28.

    Jones B, Renaut RW, Konhauser KO. Genesis of large siliceous stromatolites at Frying Pan Lake Waimangu geothermal field North Island New Zealand. Sedimentology. 2005;52:1229–52.

  29. 29.

    Power JF, Carere CR, Lee CK, Wakerley GLJ, Evans DW, Button M, et al. Microbial biogeography of 1000 geothermal springs in New Zealand. bioRxiv. 2018;247759

  30. 30.

    Barns SM, Fundyga RE, Jeffries MW, Pace NR. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc Natl Acad Sci USA. 1994;91:1609–13.

  31. 31.

    Krienitz L, Bock C, Kotut K, Luo W. Picocystis salinarum (Chlorophyta) in saline lakes and hot springs of East Africa. Phycologia. 2012;51:22–32.

  32. 32.

    Ovrutsky AR, Chan ED, Kartalija M, Bai X, Jackson M, Gibbs S, et al. Cooccurrence of free-living amoebae and nontuberculous Mycobacteria in hospital water networks and preferential growth of Mycobacterium avium in Acanthamoeba lenticulata. Appl Environ Microbiol. 2013;79:3185–92.

  33. 33.

    Baumgartner M, Stetter KO, Foissner W. Morphological Small Subunit rRNA and Physiological Characterization of Trimyema minutum (), an anaerobic ciliate from submarine hydrothermal vents growing from 28 °C to 52 °C. J Euk Microbiol. 2002;49:227–38.

  34. 34.

    Schmidtke A, Bell EM, Weithoff G. Potential grazing impact of the mixotrophic flagellate Ochromonas sp.(Chrysophyceae) on bacteria in an extremely acidic lake. J Plankton Res. 2006;28:991–1001.

  35. 35.

    Nealson KH. The limits of life on Earth and searching for life on Mars. J Geophys Res: Planets. 1997;102(E10):23675–86.

  36. 36.

    Lauber CL, Hamady M, Knight R, Fierer N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol. 2009;75:5111–20.

  37. 37.

    Packroff G, Woelfl S. A review on the occurrence and taxonomy of heterotrophic protists in extreme acidic environments of pH values ≤ 3. Hydrobiologia. 2000;433:153–6.

  38. 38.

    DeNicola DM. A review of diatoms found in highly acidic environments. Hydrobiologia. 2000;433:111–22.

  39. 39.

    Macalady JL, Jones DS, Lyon EH. Extremely acidic pendulous cave wall biofilms from the Frasassi cave system, Italy. Environ Microbiol. 2007;9:1402–14.

  40. 40.

    Hetzer A, McDonald IR, Morgan HW. Venenivibrio stagnispumantis gen. nov. sp. nov. a thermophilic hydrogen-oxidizing bacterium isolated from Champagne Pool Waiotapu, New Zealand. Int J Syst Evol Microbiol. 2008;58:398–403.

  41. 41.

    Hahn MW, Höfle MG. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol. 2001;35:113–21.

  42. 42.

    Sherr EB, Sherr BF. Significance of predation by protists in aquatic microbial food webs. A Van Leeuw J Microb. 2002;81:293–308.

  43. 43.

    Archer SDJ, McDonald IR, Herbold CW, Cary SC. Characterisation of bacterioplankton communities in the meltwater ponds of Bratina Island Victoria Land Antarctica. FEMS Microbiol Ecol. 2014;89:451–64.

  44. 44.

    Hugerth LW, Muller EE, Hu YO, Lebrun LA, Roume H, Lundin D, et al. Systematic design of 18S rRNA gene primers for determining eukaryotic diversity in microbial consortia. PLoS One. 2014;9:e95567.

  45. 45.

    Leff JW. 2016. https://github.com/leffj/helper-code-for-uparse Accessed March 2017.

  46. 46.

    Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.

  47. 47.

    Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.

  48. 48.

    Nebel M, Pfabel C, Stock A, Dunthorn M, Stoeck T. Delimiting operational taxonomic units for assessing ciliate environmental diversity using small‐subunit rRNA gene sequences. Env Microbiol Rep. 2011;3:154–8.

  49. 49.

    Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2012;41:D597–604.

  50. 50.

    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.

  51. 51.

    Venables WN, Ripley BD. Modern Applied Statistics with S. New York: Springer; 2002.

  52. 52.

    Grömping U. Relative importance for linear regression in R: the package relaimpo. J Stat Softw. 2006;17:1–27.

  53. 53.

    Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB. 2016 Vegan: community ecology package R package version 2.4-1. https://CRAN.R-project.org/package=vegan. Accessed November 2016.

  54. 54.

    Goslee SC, Urban DL. The ecodist package for dissimilarity-based analysis of ecological data. J of Stat Softw. 2007;22:1–9.

  55. 55.

    Gong J, Dong J, Liu X, Massana R. Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of oligotrich and peritrich ciliates. Protist. 2013;164:369–79.

  56. 56.

    Roberts DW, Roberts MD. Package labdsv: Ordination and Multivariate Analysis for Ecology. 2016; R package version 1.8.0.

  57. 57.

    Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.

  58. 58.

    Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3.

  59. 59.

    Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PloS ONE. 2010;5:e9490.

  60. 60.

    Asnicar F, Weingart G, Tickle TL, Huttenhower C, Segata N. Compact graphical representation of phylogenetic data and metadata with GraPhlAn. PeerJ. 2015;3:e1029.

  61. 61.

    Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. ICWSM. 2009;8:361–2.

  62. 62.

    Blondel VD, Guillaume JL, Lambiotte R, Lefebvre E. Fast unfolding of communities in large networks. J Stat Mech. 2008;2008:P10008.

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Acknowledgements

We thank Karen Houghton, Carlo Carere, Hanna-Annette Peach and David Evans for assistance with sample collection and Jessica Henley, Roanna Richards-Babbage, and Georgia Wakerley for assistance with laboratory work. We thank Lauren Shoemaker, Amber Churchill, and Manuel Delgado-Baquerizo for valuable comments. This project was funded by an NSF Graduate Research Fellowship, NSF EAPSI Fellowship, and Lewis and Clark Fund Scholarship to AMO, and MBIE grant C05X1205 to JFP, SCC, and MBS.

Author contributions

AMO, NF, MBS, and SCC designed and performed the research analyzed the data. AMO and NF wrote the manuscript with aid from AW, MBS, SCC, and JFP.

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Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    • Angela M. Oliverio
    •  & Noah Fierer
  2. Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO, 80309, USA

    • Angela M. Oliverio
    •  & Noah Fierer
  3. Extremophile Research Group, GNS Science, Private Bag 2000, Taupō, 3352, New Zealand

    • Jean F. Power
    •  & Matthew B. Stott
  4. Thermophile Research Unit, School of Science, University of Waikato, Private Bag 3105, Hamilton, 3240, New Zealand

    • Jean F. Power
    •  & S. Craig Cary
  5. Department of Microbiology and Immunology, Montana State University, Bozeman, MT, 59717, USA

    • Alex Washburne

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Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Noah Fierer.

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https://doi.org/10.1038/s41396-018-0104-2

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