Rain-Fed Granite Rock Basins Accumulate a High Diversity of Dormant Microbial Eukaryotes

A Correction to this article is available

This article has been updated

Abstract

Rain fed granite rock basins are ancient geological landforms of worldwide distribution and structural simplicity. They support habitats that can switch quickly from terrestrial to aquatic along the year. Diversity of animals and plants, and the connexion between communities in different basins have been widely explored in these habitats, but hardly any research has been carried out on microorganisms. The aim of this study is to provide the first insights on the diversity of eukaryotic microbial communities from these environments. Due to the ephemeral nature of these aquatic environments, we predict that the granitic basins should host a high proportion of dormant microeukaryotes. Based on an environmental DNA diversity survey, we reveal diverse communities with representatives of all major eukaryotic taxonomic supergroups, mainly composed of a diverse pool of low abundance OTUs. Basin communities were very distinctive, with alpha and beta diversity patterns non-related to basin size or spatial distance respectively. Dissimilarity between basins was mainly characterised by turnover of OTUs. The strong microbial eukaryotic heterogeneity observed among the basins may be explained by a complex combination of deterministic factors (diverging environment in the basins), spatial constraints, and randomness including founder effects. Most interestingly, communities contain organisms that cannot coexist at the same time because of incompatible metabolic requirements, thus suggesting the existence of a pool of dormant organisms whose activity varies along with the changing environment. These organisms accumulate in the pools, which turns granitic rock into high biodiversity microbial islands whose conservation and study deserve further attention.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Change history

  • 23 December 2019

    The original version of this article contained an erratum of omission in the Acknowledgments section.

References

  1. 1.

    Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. https://doi.org/10.1038/nature05202

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Zubkov MV, Tarran GA (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455:224–226. https://doi.org/10.1038/nature07236

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Weisse T, Anderson R, Arndt H, Calbet A, Hansen PJ, Montagnes DJS (2016) Functional ecology of aquatic phagotrophic protists – concepts, limitations, and perspectives. Eur. J. Protistol. 55:50–74. https://doi.org/10.1016/j.ejop.2016.03.003

    Article  PubMed  Google Scholar 

  4. 4.

    Field CB, Behrenfeld MJ, Randerson JT, Falkowski PG (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240. https://doi.org/10.1126/science.281.5374.237

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Esteban GF, Finlay BJ, Warren A (2015) Free-living protozoa. In: Thorp JH, Rogers DC (eds) Freshwater invertebrates: ecology and general biology4th edn. Academic Press, San Diego, pp 113–132Thorp and Covich’s

    Google Scholar 

  6. 6.

    Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545. https://doi.org/10.1038/nature12901

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Lennon J, Jones S (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nature Rev Microbiol 9:119–130. https://doi.org/10.1038/nrmicro2504

    CAS  Article  Google Scholar 

  8. 8.

    Martiny JBH, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreås L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nature Rev Microbiol 4:102–112. https://doi.org/10.1038/nrmicro1341

    CAS  Article  Google Scholar 

  9. 9.

    Grattepanche JD, Santoferrara LF, McManus GB, Katz LA (2014) Diversity of diversity: conceptual and methodological differences in biodiversity estimates of eukaryotic microbes as compared to bacteria. Trends Microbiol. 22:432–437. https://doi.org/10.1016/j.tim.2014.04.006

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Debroas D, Domaizon I, Humbert JF, Jardillier L, Lepere C, Oudart A, Tai N (2017) Overview of freshwater microbial eukaryotes diversity: a first analysis of publicly available metabarcoding data. FEMS Microbiol. Ecol. 93(4). https://doi.org/10.1093/femsec/fix023

  11. 11.

    Pompanon F, Coissac E, Taberlet P (2011) Metabarcoding a new way to analyze biodiversity. Biofutur 30:30–32

    Google Scholar 

  12. 12.

    Amaral-Zettler LA, McCliment EA, Ducklow HW, Huse SM (2009) A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA genes. PLoS One 4(7):e6372. https://doi.org/10.1371/journal.pone.0006372

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol. Ecol. 19:21–31. https://doi.org/10.1111/j.1365-294X.2009.04480.x

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, Bowser SS, Cepicka I, Decelle J, Dunthorn M, Fiore-Donno AM, Gile GH, Holzmann M, Jahn R, Jirků M, Keeling PJ, Kostka M, Kudryavtsev A, Lara E, Lukeš J, Mann DG, Mitchell EA, Nitsche F, Romeralo M, Saunders GW, Simpson AG, Smirnov AV, Spouge JL, Stern RF, Stoeck T, Zimmermann J, Schindel D, de Vargas C (2012) CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol. 10(11):e1001419. https://doi.org/10.1371/journal.pbio.1001419

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Caron DA, Hu SK (2019) Are we overestimating protistan diversity in nature? Trends Microbiol. 27(3):197–205. https://doi.org/10.1016/j.tim.2018.10.009

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    de Vargas S, Audic N, Henry J et al (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:1261605. https://doi.org/10.1126/science.1261605

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    del Campo J, Guillou L, Hehenberger E, Logares R, López-García P, Massana R (2016) Ecological and evolutionary significance of novel protist lineages. Eur. J. Protistol. 55:4–11. https://doi.org/10.1016/j.ejop.2016.02.002

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Logares R, Mangot JF, Massana R (2015) Rarity in aquatic microbes: placing protists on the map. Res. Microbiol. 166:831–841. https://doi.org/10.1016/j.resmic.2015.09.009

    Article  PubMed  Google Scholar 

  19. 19.

    Green JL, Holmes AJ, Westoby M, Oliver I, Briscoe D, Dangerfield M, Gillings M, Beattie AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432:747–750. https://doi.org/10.1038/nature03034

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Lepère C, Domaizon I, Taïb N, Mangot JF, Bronner G, Boucher D, Debroas D (2013) Geographic distance and ecosystem size determine the distribution of smallest protists in lacustrine ecosystems. FEMS Microbiol. Ecol. 85:85–94. https://doi.org/10.1111/1574-6941.12100

    Article  PubMed  Google Scholar 

  21. 21.

    Wu B, Tian J, Bai C, Xiang M, Sun J, Liu X (2013) The biogeography of fungal communities in wetland sediments along the Changjiang River and other sites in China. ISME J l7:1299–1309. https://doi.org/10.1038/ismej.2013.29

    CAS  Article  Google Scholar 

  22. 22.

    Barreto DP, Conrad R, Klose M, Claus P, Enrich-Prast A (2014) Distance-decay and taxa-area relationships for bacteria, archaea and methanogenic archaea in a tropical lake sediment. PLoS One 9(10):e110128. https://doi.org/10.1371/journal.pone.0110128

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Hendershot JN, Read QD, Henning JA, Sanders NJ, Classen AT (2017) Consistently inconsistent drivers of microbial diversity and abundance at macroecological scales. Ecology 98:1757–1763. https://doi.org/10.1002/ecy.1829

    Article  PubMed  Google Scholar 

  24. 24.

    Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol. Lett. 7(12):1225–1241. https://doi.org/10.1111/j.1461-0248.2004.00684.x

    Article  Google Scholar 

  25. 25.

    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton

    Google Scholar 

  26. 26.

    Coleman BD (1981) Random placement and species–area relations. Math. Biosci. 54:191–215

    Article  Google Scholar 

  27. 27.

    Boileau MG, Hebert PDN, Schwartz SS (1992) Nonequilibrium gene frequency divergence: persistent founder effects in natural populations. J. Evol. Biol. 5:25–39

    Article  Google Scholar 

  28. 28.

    Reith F, Zammit CM, Pohrib R, Gregg AL, Wakelin SA (2015) Geogenic factors as drivers of microbial community diversity in soils overlying polymetallic deposits. Appl. Environ. Microbiol. 81:7822–7832. https://doi.org/10.1128/AEM.01856-15

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Simon M, Jardillier L, Deschamps P, Moreira D, Restoux G, Bertolino P, López-García P (2015) Complex communities of small protists and unexpected occurrence of typical marine lineages in shallow freshwater systems. Environ. Microbiol. 17:3610–3627. https://doi.org/10.1111/1462-2920.12591

    Article  PubMed  Google Scholar 

  30. 30.

    Simon M, Lopez-Garcia P, Deschamps P et al (2015) Marked seasonality and high spatial variability of protist communities in shallow freshwater systems. ISME J 9:1941–1953. https://doi.org/10.1038/ismej.2015.6

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Sisson C, Gulla-Devaney B, Katz LA, Grattepanche JD (2018) Seed bank and seasonal patterns of the eukaryotic SAR (Stramenopila, Alveolata and Rhizaria) clade in a New England vernal pool. J. Plankton Res. 40:376–390. https://doi.org/10.1093/plankt/fby020

    Article  Google Scholar 

  32. 32.

    Twidale CR (1982) Granite landforms. Elsevier Scientific Publishing Company, Amsterdam, 359 pp

    Google Scholar 

  33. 33.

    Brendonck L, Lanfranco S, Timms B, Vanschoenwinkel B (2016) Invertebrates in rock pools. In: Batzer D, Boix D (eds) Invertebrates in freshwater wetlands. Springer International Publishing, Cham, pp 25–53

    Google Scholar 

  34. 34.

    Jocque M, Vanschoenwinkel B, Brendonck L (2010) Freshwater rock pools: a review of habitat characteristics, faunal diversity and conservation value. Freshw. Biol. 55:1587–1602. https://doi.org/10.1111/j.1365-2427.2010.02402.x

    Article  Google Scholar 

  35. 35.

    Anusa A, Ndagurwa HGT, Magadza CHD (2012) The influence of pool size on species diversity and water chemistry in temporary rock pools on Domboshawa Mountain, northern Zimbabwe. Afr. J. Aquat. Sci. 37(1):89–99. https://doi.org/10.2989/16085914.2012.666378

    CAS  Article  Google Scholar 

  36. 36.

    Reed GB, Klugh AB (1924) The correlation between hydrogen-ion concentration and the biota of granite and limestone pools. Ecology 5:272–275

    CAS  Article  Google Scholar 

  37. 37.

    Pinder AM, Halse SA, Shiel RJ, McRae JM (2000) Granite outcrop pools in south-western Australia: foci of diversification and refugia for aquatic invertebrates. J. R. Soc. West. Aust. 83:149–161

    Google Scholar 

  38. 38.

    Rylander K (2011) Protists and invertebrates in temporary pools on enchanted rock, Llano County, Texas: 1965 and 2010. The Free Library. Texas Academy of Science. https://www.thefreelibrary.com/Protists+and+invertebrates+in+temporary+pools+on+Enchanted+Rock%2c...-a0382319889. Accessed 9 Dec 2016

  39. 39.

    Mahé F, de Vargas C, Bass D, Czech L, Stamatakis A, Lara E, Singer D, Mayor J, Bunge J, Sernaker S, Siemensmeyer T, Trautmann I, Romac S, Berney C, Kozlov A, Mitchell EAD, Seppey CVW, Egge E, Lentendu G, Wirth R, Trueba G, Dunthorn M (2017) Parasites dominate hyperdiverse soil protist communities in Neotropical rainforests. Nat Ecol Evol 1:0091. https://doi.org/10.1038/s41559-017-0091

    Article  Google Scholar 

  40. 40.

    IGME (2017) Mapa Geológico Nacional. Instituto Geológico y Minero de España http://info.igme.es/visorweb/ Accessed 20 June 2018

  41. 41.

    García-Rodríguez M, Gómez-Heras M, Álvarez de Buergo M, Fort R, Aroztegui J (2015) Polygonal cracking associated to vertical and subvertical fracture surfaces in granite (La Pedriza del Manzanares, Spain): considerations for a morphological classification. J. Iber. Geol. 41(3):365–383. https://doi.org/10.5209/rev_JIGE.2015.v41.n3.48860

    Article  Google Scholar 

  42. 42.

    Domínguez Villar D (2007) Análisis morfométrico de pilancones: consideraciones genéticas, evolutivas y paleoambientales. Dissertation 336 pp. UCM. Madrid

  43. 43.

    Hadziavdic K, Lekang K, Lanzen A, Jonassen I, Thompson EM, Troedsson C (2014) Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS One 9:e87624. https://doi.org/10.1371/journal.pone.0087624

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Schiaffino MR, Lara E, Fernández L, Balagué V, Singer D, Seppey CW, Massana R, Izaguirre I (2016) Microbial eukaryote communities exhibit robust biogeographical patterns along a gradient of Patagonian and Antarctic lakes. Environ. Microbiol. 18(12):5249–5264. https://doi.org/10.1111/1462-2920.13566

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48(3):443–453

    CAS  Article  Google Scholar 

  46. 46.

    Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, Boutte C, Burgaud G, de Vargas C, Decelle J, del Campo J, Dolan JR, Dunthorn M, Edvardsen B, Holzmann M, Kooistra WH, Lara E, le Bescot N, Logares R, Mahé F, Massana R, Montresor M, Morard R, Not F, Pawlowski J, Probert I, Sauvadet AL, Siano R, Stoeck T, Vaulot D, Zimmermann P, Christen R (2013) The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41:597–604. https://doi.org/10.1093/nar/gks1160

    CAS  Article  Google Scholar 

  47. 47.

    Mahé F, Rognes T, Quince C, de Vargas C, Dunthorn M (2014) Swarm: robust and fast clustering method for amplicon-based studies. Peer J 2:e593. https://doi.org/10.7717/peerj.593

    Article  PubMed  Google Scholar 

  48. 48.

    Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand. J. Stat. 11:265–270

    Google Scholar 

  49. 49.

    Gotelli NJ, Colwell RK (2011) Estimating species richness. In: Magurran AE, McGill BJ (eds) Frontiers in measuring biodiversity. Oxford University Press, New York, pp 39–54

    Google Scholar 

  50. 50.

    Simpson EH (1949) Measurements of diversity. Nature 163:688. https://doi.org/10.1038/163688a0

    Article  Google Scholar 

  51. 51.

    Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  52. 52.

    Pielou EC (1966) The measurement of diversity in different types of biological collection. J. Theor. Biol. 13:131–144

    Article  Google Scholar 

  53. 53.

    Oksanen F, Blanchet G, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2015) Community ecology package version 2.3-1. Date 2015-09-24. 285 pp

  54. 54.

    Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 19(1):134–143. https://doi.org/10.1111/j.1466-8238.2009.00490.x

    Article  Google Scholar 

  55. 55.

    Baselga A (2013) Separating the two components of abundance-based dissimilarity: balanced changes in abundance vs. abundance gradients. Methods Ecol. Evol. 4:552–557. https://doi.org/10.1111/2041-210X.12029

    Article  Google Scholar 

  56. 56.

    Gómez-Rodríguez C, Baselga A (2018) Variation among European beetle taxa in patterns of distance decay of similarity suggests a major role of dispersal processes. Ecography 41:1–10. https://doi.org/10.1111/ecog.03693

    Article  Google Scholar 

  57. 57.

    Fontaneto D, Eckert EM, Anicic N, Lara E, Mitchell EAD (2019) We are ready for faunistic surveys of bdelloid rotifers through DNA barcoding: the example of Sphagnum bogs of the Swiss Jura Mountains. Limnetica 38:213–225. https://doi.org/10.23818/limn.38.02

    Article  Google Scholar 

  58. 58.

    Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, Cárdenas P, Čepička I, Chistyakova L, del Campo J, Dunthorn M, Edvardsen B, Eglit Y, Guillou L, Hampl V, Heiss AA, Hoppenrath M, James TY, Karnkowska A, Karpov S, Kim E, Kolisko M, Kudryavtsev A, Lahr DJG, Lara E, le Gall L, Lynn DH, Mann DG, Massana R, Mitchell EAD, Morrow C, Park JS, Pawlowski JW, Powell MJ, Richter DJ, Rueckert S, Shadwick L, Shimano S, Spiegel FW, Torruella G, Youssef N, Zlatogursky V, Zhang Q (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66(1):4–119. https://doi.org/10.1111/jeu.12691

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Simon M, Lopez-Garcıa P, Deschamps P, Restoux G, Bertolino P, Moreira D, Jardillier L (2016) Resilience of freshwater communities of small microbial eukaryotes undergoing severe drought events. Front. Microbiol. 7:812. https://doi.org/10.3389/fmicb.2016.00812

    Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Brendonck L, Jocque M, Hulsmans A, Vanschoenwinkel B (2010) Pools ‘on the rocks’: freshwater rock pools as model system in ecological and evolutionary research. Limnetica 29:25–40

    Google Scholar 

  61. 61.

    Meier S, Soininen J (2014) Phytoplankton metacommunity structure in subarctic rock pools. Aquat. Microb. Ecol. 73:81–91. https://doi.org/10.3354/ame01711

    Article  Google Scholar 

  62. 62.

    Bengtsson J, Ebert D (1998) Distributions and impacts of microparasites on Daphnia in a rock pool metapopulation. Oecologia 115:213–221. https://doi.org/10.1007/s004420050510

    Article  PubMed  Google Scholar 

  63. 63.

    Bass D, Cavalier-Smith T (2004) Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). Int. J. Syst. Evol. Microbiol. 54:2393–2404. https://doi.org/10.1099/ijs.0.63229-0

    CAS  Article  PubMed  Google Scholar 

  64. 64.

    Fiore-Donno AM, Rixen C, Rippin M, Glaser K, Samolov E, Karsten U, Becker B, Bonkowski M (2018) New barcoded primers for efficient retrieval of cercozoan sequences in high-throughputenvironmental diversity surveys, with emphasis on world-wide biological soil crusts. Mol. Ecol. Resour. 18(2):229–239. https://doi.org/10.1111/1755-0998.12729

    CAS  Article  PubMed  Google Scholar 

  65. 65.

    Harder CB, Rønn R, Brejnrod A, Bass D, Al-Soud WA, Ekelund F (2016) Local diversity of heathland Cercozoa explored by in-depth sequencing. ISME J 10:2488–2497. https://doi.org/10.1038/ismej.2016.31

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Howe AT, Bass D, Vickerman K, Chao EE, Cavalier-Smith T (2009) Phylogeny, taxonomy, and astounding genetic diversity of Glissomonadida ord. nov., the dominant gliding Zooflagellates in soil (Protozoa: Cercozoa). Protist 160:159–189. https://doi.org/10.1016/j.protis.2008.11.007

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Ekelund F (1996) Growth kinetics of five common heterotrophic soil flagellates. Eur. J. Soil Biol. 32:15–24

    Google Scholar 

  68. 68.

    Hess S, Melkonian M (2013) The mystery of clade X: Orciraptor gen. nov and Viridiraptor gen. nov are highly specialised, algivorous amoeboflagellates (Glissomonadida, Cercozoa). Protist 164:706–747. https://doi.org/10.1016/j.protis.2013.07.003

    Article  PubMed  Google Scholar 

  69. 69.

    Seppey CVW, Singer D, Dumack K, Fournier B, Belbahri L, Mitchell EAD, Lara E (2017) Distribution patterns of soil microbial eukaryotes suggests widespread algivory by phagotrophic protists as an alternative pathway for nutrient cycling. Soil Biol. Biochem. 112:68–76. https://doi.org/10.1016/j.soilbio.2017.05.002

    CAS  Article  Google Scholar 

  70. 70.

    Beyond the human eye. http://beyondthehumaneye.blogspot.com/2009/07/ Accessed 20 th June 2019

  71. 71.

    Kaštovský J (2008) A report of Stephanosphaera pluvialis COHN 1852 (Chlorophyta, Chlamydophyceae). Fottea 8:109–110. https://doi.org/10.5507/fot.2008.006

    Article  Google Scholar 

  72. 72.

    Saad JF, Schiaffino MR, Vinocur A, O'Farrell I, Tell G, Izaguirre I (2013) Microbial planktonic communities of freshwater environments from Tierra del Fuego: dominant trophic strategies in lakes with contrasting features. J. Plankton Res. 35:1220–1233. https://doi.org/10.1093/plankt/fbt075

    CAS  Article  Google Scholar 

  73. 73.

    Correll D (1998) The role of phosphorus in the eutrophication of receiving waters: a review. J. Environ. Qual. 27:261–266

    CAS  Article  Google Scholar 

  74. 74.

    Carlson RE (1977) A trophic state index for lakes. Limnol. Oceanogr. 22:361–369. https://doi.org/10.4319/lo.1977.22.2.0361

    CAS  Article  Google Scholar 

  75. 75.

    Kolodziej K, Stoeck T (2007) Cellular identification of a novel uncultured marine stramenopile (MAST-12 clade) small-subunit rRNA gene sequence from a Norwegian estuary by use of fluorescence in situ hybridization-scanning electron microscopy. Appl. Environ. Microbiol. 73(8):2718–2726. https://doi.org/10.1128/AEM.02158-06

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Lara E, Mitchell EAD, Moreira D, López-García P (2011) Highly diverse and seasonally dynamic protist community in a pristine peat bog. Protist 162:14–32. https://doi.org/10.1016/j.protis.2010.05.003

    Article  PubMed  Google Scholar 

  77. 77.

    Massana R, del Campo J, Sieracki ME, Audic S, Logares R (2014) Exploring the uncultured microeukaryote majority in the oceans: reevaluation of ribogroups within stramenopiles. ISME J 8:854–866. https://doi.org/10.1038/ismej.2013.204

    Article  PubMed  Google Scholar 

  78. 78.

    Bernard C, Simpson AGB, Patterson DJ (2000) Some free-living flagellates (Protista) from anoxic habitats. Ophelia 52:113–142. https://doi.org/10.1080/00785236.1999.10409422

    Article  Google Scholar 

  79. 79.

    Lara E, Acosta-Mercado D (2012) A molecular perspective on ciliates as soil bioindicators. Eur. J. Soil Biol. 49:107–111. https://doi.org/10.1016/j.ejsobi.2011.11.001

    CAS  Article  Google Scholar 

  80. 80.

    Bourland W, Rotterová J, Čepička I (2018) Morphologic and molecular characterization of Brachonella pulchra (Kahl, 1927) comb. nov. (Armophorea, Ciliophora) with comments on cyst structure and formation. Int. J. Syst. Evol. Microbiol. 68(9):3052–3065. https://doi.org/10.1099/ijsem.0.002888

    CAS  Article  PubMed  Google Scholar 

  81. 81.

    Galand PE, Casamayor EO, Kirchman DL, Love JC (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc. Natl. Acad. Sci. U. S. A. 106(52):22427–22432. https://doi.org/10.1073/pnas.0908284106

    Article  PubMed  PubMed Central  Google Scholar 

  82. 82.

    Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored rare biosphere. Proc. Natl. Acad. Sci. U. S. A. 103:12115–12120. https://doi.org/10.1073/pnas.0605127103

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Dunthorn M, Stoeck T, Clamp J, Warren A, Mahé F (2014) Ciliates and the rare biosphere: a review. J. Eukaryot. Microbiol. 61:404–409. https://doi.org/10.1111/jeu.12121

    Article  PubMed  Google Scholar 

  84. 84.

    Debroas D, Hugoni M, Domaizon I (2015) Evidence for an active rare biosphere within freshwater protists community. Mol. Ecol. 24:1236–1247. https://doi.org/10.1111/mec.13116

    CAS  Article  PubMed  Google Scholar 

  85. 85.

    Weisse T (2014) Ciliates and the rare biosphere – community ecology and population dynamics. J. Eukaryot. Microbiol. 61(4):419–433. https://doi.org/10.1111/jeu.12123

    Article  PubMed  Google Scholar 

  86. 86.

    Jousset A, Bienhold C, Chatzinotas A, Gallien L, Gobet A, Kurm V, Küsel K, Rillig MC, Rivett DW, Salles JF, van der Heijden M, Youssef NH, Zhang X, Wei Z, Hol WH (2017) Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J 11:853–862. https://doi.org/10.1038/ismej.2016.174

    Article  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Pillet L, Fontaine D, Pawlowski J (2012) Intra-genomic ribosomal RNA polymorphism and morphological variation in Elphidium macellum suggests inter-specific hybridization in foraminifera. PLoS One 7:e32373. https://doi.org/10.1371/journal.pone.0032373

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Kudryavtsev A, Gladkikh A (2017) Two new species of Ripella (Amoebozoa, Vannellida) and unusual intragenomic variability in the SSU rRNA gene of this genus. Eur. J. Protistol. 61:92–106. https://doi.org/10.1016/j.ejop.2017.09.003

    Article  PubMed  Google Scholar 

  89. 89.

    Miranda LN, Zhuang YY, Zhang H, Lin S (2012) Phylogenetic analysis guided by intragenomic SSU rDNA polymorphism refines classification of “Alexandrium tamarense” species complex. Harmful Algae 16:35–48. https://doi.org/10.1016/j.hal.2012.01.002

    CAS  Article  Google Scholar 

  90. 90.

    Ganley ARD, Kobayashi T (2007) Highly efficient concerted evolution in the ribosomal DNA repeats: Total rDNA repeat variation revealed by whole-genome shotgun sequence data. Genome Res. 17:184–191. https://doi.org/10.1101/gr.5457707

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  91. 91.

    De Meester L, Declerck S, Stoks R, Louette G, Van De Meutter F, De Bie T, Michels E, Brendonck L (2005) Ponds and pools as model systems in conservation biology, ecology and evolutionary biology. Aquat. Conserv. 15:715–725. https://doi.org/10.1002/aqc.748

    Article  Google Scholar 

  92. 92.

    Brendonck L, De Meester L, Riddoch BJ (2000) Regional structuring of genetic variation in short-lived rock pool populations of Branchipodopsis wolfi (Crustacea: Anostraca). Oecologia 123:506–515

    CAS  Article  Google Scholar 

  93. 93.

    Sassenhagen I, Wilken S, Godhe A, Rengefors K (2015) Phenotypic plasticity and differentiation in an invasive freshwater microalga. Harmful Algae 41:38–45. https://doi.org/10.1016/j.hal.2014.11.001

    Article  Google Scholar 

  94. 94.

    Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems4th edn. Blackwell Publishing Ltd., p 750

  95. 95.

    Ren H, Yuan X, Yue J, Wang X, Liu H (2016) Potholes of mountain river as biodiversity spots: structure and dynamics of the benthic invertebrate community. Pol. J. Ecol. 64(1):70–83. https://doi.org/10.3161/15052249pje2016.64.1.007

    Article  Google Scholar 

  96. 96.

    Soininen J, Luoto M (2012) Is catchment productivity a useful predictor of taxa richness in lake plankton communities? Ecol. Appl. 22:624–633. https://doi.org/10.1890/11-1126.1

    Article  PubMed  Google Scholar 

  97. 97.

    Therriault TW, Kolasa J (2001) Desiccation frequency reduces species diversity and predictability of community structure in coastal rock pools. Isr J Zool 47(4):477–489

    Article  Google Scholar 

  98. 98.

    Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J. Biogeogr. 26:867–878. https://doi.org/10.1046/j.1365-2699.1999.00305.x

    Article  Google Scholar 

Download references

Acknowledgements

Permits to collect samples and facilities provided by The Parque Nacional Sierra de Guadarrama are gratefully acknowledged.

Funding

This study was funded by Ministerio de Economía y Competitividad (MINECO-Spain), Project MICROEPICS (Ref: CGL2013-40851-P/ BOS 2014-2018; PI: MM-C). EL was funded by a project “Atraccion de talento investigador” by the Consejería de Educación, Juventud y Deporte, Comunidad de Madrid (Spain) 2017-T1/AMB-5210 and by a grant from the Swiss National Foundation for Research SNF 31003A_143960.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Mercedes Martín-Cereceda.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Enrique Lara and Mercedes Martin-Cereceda share last co-authorship

Electronic Supplementary Material

ESM 1

(XLSX 247 kb).

ESM 2

(DOCX 15 kb).

ESM 3

(DOCX 47 kb).

ESM 4

(PDF 1647 kb).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Velasco-González, I., Sanchez-Jimenez, A., Singer, D. et al. Rain-Fed Granite Rock Basins Accumulate a High Diversity of Dormant Microbial Eukaryotes. Microb Ecol 79, 882–897 (2020). https://doi.org/10.1007/s00248-019-01463-y

Download citation

Keywords

  • Granite rock basins
  • Microbial reservoirs
  • Protists
  • Fungi
  • Dormancy
  • Conservation