Microbial Ecology

, Volume 68, Issue 3, pp 504–518 | Cite as

Pioneer Microbial Communities of the Fimmvörðuháls Lava Flow, Eyjafjallajökull, Iceland

  • Laura C. Kelly
  • Charles S. Cockell
  • Thorsteinn Thorsteinsson
  • Viggó Marteinsson
  • John Stevenson
Environmental Microbiology

Abstract

Little is understood regarding the phylogeny and metabolic capabilities of the earliest colonists of volcanic rocks, yet these data are essential for understanding how life becomes established in and interacts with the planetary crust, ultimately contributing to critical zone processes and soil formation. Here, we report the use of molecular and culture-dependent methods to determine the composition of pioneer microbial communities colonising the basaltic Fimmvörðuháls lava flow at Eyjafjallajökull, Iceland, formed in 2010. Our data show that 3 to 5 months post eruption, the lava was colonised by a low-diversity microbial community dominated by Betaproteobacteria, primarily taxa related to non-phototrophic diazotrophs such as Herbaspirillum spp. and chemolithotrophs such as Thiobacillus. Although successfully cultured following enrichment, phototrophs were not abundant members of the Fimmvörðuháls communities, as revealed by molecular analysis, and phototrophy is therefore not likely to be a dominant biogeochemical process in these early successional basalt communities. These results contrast with older Icelandic lava of comparable mineralogy, in which phototrophs comprised a significant fraction of microbial communities, and the non-phototrophic community fractions were dominated by Acidobacteria and Actinobacteria.

Supplementary material

248_2014_432_Fig6_ESM.gif (102 kb)
Fig. 1

Principal component analysis (PCA) of bacterial communities based 16S rRNA gene clone libraries. PCA was performed on operational taxonomic unit (OTU) abundance data in MOTHUR. (GIF 102 kb)

248_2014_432_MOESM1_ESM.tif (1008 kb)
High Resolution Image (TIFF 1,008 kb)
248_2014_432_MOESM2_ESM.doc (30 kb)
Table S2(DOC 30 KB)

References

  1. 1.
    Berner RA (1993) Weathering and its effect on atmospheric CO2 over Phanerozoic time. Chem Geol 107:373–374. doi:10.1016/0009-2541(93)90212-2 CrossRefGoogle Scholar
  2. 2.
    Gaillardet J, Dupre P, Louvat CJ, Allègre CJ (1999) Global silicate weathering and CO2 consumption rates deduced from the chemistry of the large rivers. Chem Geol 159:3–30. doi:10.1016/S0009-2541(99)00031-5 CrossRefGoogle Scholar
  3. 3.
    Dessert C, Dupre B, Francois LM (2001) Erosion of Deccan Traps determined by river geochemistry: impact on the global climate and the 87Sr/86Sr ratio of seawater. Earth Planet Sc Lett 188:459–474. doi:10.1016/S0012-821X(01)00317-X CrossRefGoogle Scholar
  4. 4.
    Dessert C, Dupré B, Gaillardet J, François LM, Allègre CJ (2003) Basalt weathering laws and the impact of basalt weathering on the global carbon cycle. Chem Geol 202:257–273. doi:10.1016/j.chemgeo.2002.10.001 CrossRefGoogle Scholar
  5. 5.
    Bland W, Rolls D (2005) Weathering: an introduction to the scientific principles. Arnold, LondonGoogle Scholar
  6. 6.
    Dahlgren R, Shoji S, Nanzyo M (1993) Mineralogical characteristics of volcanic ash soils. In: Shoji S, Nanzyo M (eds) Volcanic ash soils genesis, properties, and utilization. Elsevier, Amsterdam, pp 101–143CrossRefGoogle Scholar
  7. 7.
    Vitousek PM, Ladefoged TN, Kirch PV, Hartshorn AS, Graves MW, Hotchkiss SC, Tuljapurkar S, Chadwick OA (2004) Soils, agriculture, and society in precontact Hawaii. Science 304:1665–1669. doi:10.1126/science.1099619 CrossRefPubMedGoogle Scholar
  8. 8.
    Belobrov VP, Ovechkin SV (2005) Soils and soil cover patterns of volcanic plateaus in Indochina. Eurasian Soil Sci 38:1065–1074Google Scholar
  9. 9.
    Ibekwe MA, Kennedy AC, Halvorson JJ, Yang C-H (2007) Characterization of developing microbial communities in Mount St. Helens pyroclastic substrate. Soil Biol Biochem 39:2496–2507. doi:10.1016/j.soilbio.2007.05.010 CrossRefGoogle Scholar
  10. 10.
    Herrera A, Cockell CS, Self S, Blaxter M, Reitner J, Arp G, Dröse W, Thorsteinsson T, Tindle AG (2008) Bacterial colonization and weathering of terrestrial obsidian in Iceland. Geomicrobiol J 25:25–47. doi:10.1080/01490450701828982 CrossRefGoogle Scholar
  11. 11.
    Gomez-Alvarez V, King GM, Nüsslein K (2007) Comparative bacterial diversity in recent Hawaiian volcanic deposits of different ages. FEMS Microbiol Ecol 60:60–73. doi:10.1111/j.1574-6941.2006.00253.x CrossRefPubMedGoogle Scholar
  12. 12.
    Kelly L, Cockell C, Piceno Y, Andersen G, Thorsteinsson T, Marteinsson V (2010) Bacterial diversity of weathered terrestrial Icelandic volcanic glasses. Microb Ecol 60:740–752. doi:10.1007/s00248-010-9684-8 CrossRefPubMedGoogle Scholar
  13. 13.
    Schwabe GH (1970) On the algal settlement in craters on Surtsey during summer 1968. Surtsey Research Progress Report, V:68-69Google Scholar
  14. 14.
    Kristinsson H (1970) Report on the lichenological work on Surtsey and in Iceland. Surtsey Research Progress Report V:52Google Scholar
  15. 15.
    Kristinsson H (1974) Lichen colonization in Surtsey 1971-1973. Surtsey Research Progress Report VII:9-16Google Scholar
  16. 16.
    Schwabe GH, Behre K (1972) Algae on Surtsey in 1969-1970. Surtsey Research Progress Report VI:85-89Google Scholar
  17. 17.
    Brock TD (1973) Primary colonization of Surtsey, with special reference to the blue-green algae. Oikos 24:239–243CrossRefGoogle Scholar
  18. 18.
    Englund B (1976) Nitrogen fixation by free-living microorganisms on the lava field of Heimaey, Iceland. Oikos 27:428–432. doi:10.2307/3543461 CrossRefGoogle Scholar
  19. 19.
    King GM (2003) Contributions of atmospheric CO and hydrogen uptake to microbial dynamics on recent Hawaiian volcanic deposits. Appl Environ Microb 69:4067–4075. doi:10.1128/AEM.69.7.4067-4075.2003 CrossRefGoogle Scholar
  20. 20.
    Weber CF, King GM (2010) Distribution and diversity of carbon monoxide-oxidizing bacteria and bulk bacterial communities across a succession gradient on a Hawaiian volcanic deposit. Environ Microbiol 12:1855–1867. doi:10.1111/j.1462-2920.2010.02190.x CrossRefPubMedGoogle Scholar
  21. 21.
    Kelly LC, Cockell CS, Herrera-Belaroussi A, Piceno YM, Andersen G, DeSantis TZ, Brodie E, Thorsteinsson T, Marteinsson V, Poly F, LeRoux X (2011) Bacterial diversity of terrestrial crystalline volcanic rocks, Iceland. Microb Ecol 62:69–79. doi:10.1007/s00248-011-9864-1 CrossRefPubMedGoogle Scholar
  22. 22.
    Cockell CS, Olsson-Francis K, Herrera A, Kelly L, Thorsteinsson T, Marteinsson V (2009) Bacteria in weathered basaltic glass, Iceland. Geomicrobiol J 26:491–507. doi:10.1080/01490450903061101 CrossRefGoogle Scholar
  23. 23.
    Sigmundsson F, Hreinsdóttir S, Hooper A, Árnadóttir T, Pedersen R, Roberts M, Óskarsson N, Auriac A, Decriem J, Einarsson P, Hensch M, Ófeigsson BG, Sturkell E, Sveinbjörnsson H, Feigl KL (2010) Intrusion triggering of the 2010 Eyjafjallajokull explosive eruption. Nature 468:426–430. doi:10.1038/nature09558 CrossRefPubMedGoogle Scholar
  24. 24.
    Edwards BR, Gudmundsson MT, Thordarson T, Magnússon E, Höskuldsson A, Oddsson B, Haklar JP (2012) Interactions between lava and snow/ice during the 2010 Fimmvörðuháls eruption, south-central Iceland. J Geophys Res 117, B04302. doi:10.1029/2011JB008985 Google Scholar
  25. 25.
    Ramsey MH, Potts PJ, Webb PC, Watkins P, Watson JS, Coles BJ (1995) An objective assessment of analytical method precision: comparison of ICP-AES and XRF for the analysis of silicate rocks. Chem Geol 124:1–19. doi:10.1016/0009-2541(95)00020-M CrossRefGoogle Scholar
  26. 26.
    Watson JS (1996) Fast, simple method of powder pellet preparation for x-ray fluorescence analysis. X-Ray Spectrom 25:173–174CrossRefGoogle Scholar
  27. 27.
    Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61CrossRefGoogle Scholar
  28. 28.
    Sattley WM, Madigan MT (2006) Isolation, characterization, and ecology of cold-active, chemolithotrophic, sulfur-oxidizing bacteria from perennially ice-covered Lake Fryxell, Antarctica. Appl Environ Microb 72:5562–5568. doi:10.1128/AEM.00702-06 CrossRefGoogle Scholar
  29. 29.
    Atlas RM (2004) Handbook of microbiological media. CRC Press, FloridaCrossRefGoogle Scholar
  30. 30.
    Edwards U, Rogall T, Blöcker, Emde M, Böttger E (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nuc Acids Res 17:7843–7853. doi:10.1093/nar/17.19.7843 CrossRefGoogle Scholar
  31. 31.
    Bruce KD, Hiorns WD, Hobman JL, Osborn AM, Strike P, Ritchie DA (1992) Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl Environ Microb 58:3413–3416Google Scholar
  32. 32.
    Calvaruso C, Turpault MP, Leclerc E, Ranger J, Garbaye J, Uroz S, Frey-Klett P (2010) Influence of forest trees on the distribution of mineral weathering-associated bacterial communities of the Scleroderma citrinum mycorrhizosphere. Appl Environ Microb 76:4780–4787. doi:10.1128/AEM.03040-09 CrossRefGoogle Scholar
  33. 33.
    Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microb 63:3327–3332Google Scholar
  34. 34.
    Borneman J, Hartin RJ (2000) PCR primers that amplify fungal rRNA genes from environmental samples. Appl Environ Microb 66:4356–4360. doi:10.1128/AEM.66.10.4356-4360.2000 CrossRefGoogle Scholar
  35. 35.
    Schwieger F, Tebbe C (1998) A new approach to utilize PCR-single-strand-conformation polymorphis for 16S rRNA gene-based microbial community analysis. Appl Environ Microb 64:4870–4876Google Scholar
  36. 36.
    Herrera A, Cockell CS (2007) Exploring microbial diversity in volcanic environments: a review of methods in DNA extraction. J Microbiol Meth 70:1–12. doi:10.1016/j.mimet.2007.04.005 CrossRefGoogle Scholar
  37. 37.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microb 72:5069–5072. doi:10.1128/AEM.03006-05 CrossRefGoogle Scholar
  38. 38.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing MOTHUR: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–7541. doi:10.1128/AEM.01541-09 CrossRefGoogle Scholar
  39. 39.
    Felsenstein J (1993) Phylip (phylogeny inference package) version 3.68Google Scholar
  40. 40.
    Singleton DR, Furlong MA, Rathbun SL, Whitman WB (2001) Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microb 67:4374–4376. doi:10.1128/AEM.67.9.4374-4376.2001 CrossRefGoogle Scholar
  41. 41.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb 73:5261–5267. doi:10.1128/AEM.00062-07 CrossRefGoogle Scholar
  42. 42.
    Tamura KD, Dudley J, Nei M, Kumar S (2007) Mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092 CrossRefPubMedGoogle Scholar
  43. 43.
    Le Bas MJ, Le Maitre RW, Streckeisen A, Zanettin B (1986) A chemical classification of volcanic rocks based on the total alkali–silica diagram. J Petrol 27:745–750CrossRefGoogle Scholar
  44. 44.
    Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11:783–791Google Scholar
  45. 45.
    Kaštovská K, Elster J, Stibal M, Šantrůčková H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (high Arctic). Microb Ecol 50:396–407. doi:10.1007/s00248-005-0246-4 CrossRefPubMedGoogle Scholar
  46. 46.
    Nemergut D, Anderson S, Cleveland C, Martin A, Miller A, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–122. doi:10.1007/s00248-006-9144-7 CrossRefPubMedGoogle Scholar
  47. 47.
    Henriksson LE, Henriksson E (1982) Concerning the biological nitrogen fixation on Surtsey. Surtsey Res Prog Rep IX:9–12Google Scholar
  48. 48.
    Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175. doi:10.2307/2937039 CrossRefGoogle Scholar
  49. 49.
    Duc L, Noll M, Meier B, Bürgmann H, Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding alpine glacier. Microb Ecol 57:179–190. doi:10.1007/s00248-008-9408-5 CrossRefPubMedGoogle Scholar
  50. 50.
    King GM (2007) Chemolithotrophic bacteria: distributions, functions and significance in volcanic environments. Microbes Environ 22:309–319. doi:10.1264/jsme2.22.309 CrossRefGoogle Scholar
  51. 51.
    Walker LR, del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  52. 52.
    Vaitilingom M, Deguillaume L, Vinatier V, Sancelme M, Amato P, Chaumerliac N, Delort AM (2013) Potential impact of microbial activity on the oxidant capacity and organic carbon budget in clouds. Proc Natl Acad Sci U S A 110:559–564. doi:10.1073/pnas.1205743110 PubMedCentralCrossRefPubMedGoogle Scholar
  53. 53.
    Lu H, Fujimura R, Sato Y, Nanba K, Kamijo T, Ohta H (2008) Characterization of Herbaspirillum- and Limnobacter-related strains isolated from young volcanic deposits in Miyake-Jima Island, Japan. Microbes Environ 23:66–72. doi:10.1264/jsme2.23.6 CrossRefPubMedGoogle Scholar
  54. 54.
    Heue KP, Brenninkmeijer CAM, Baker AK, Rauthe-Schöch A, Walter D, Wagner T, Hörmann C, Sihler H, Dix B, Frieß U, Platt U, Martinsson BG, van Velthoven PFJ, Zahn A, Ebinghaus R (2011) SO2 and BrO observation in the plume of Eyjafjallajökull volcano 2010: CARIBIC and GOME-2 retrievals. Atmos Chem Phys 11:2973–2989. doi:10.5194/acp-11-2973-2011 CrossRefGoogle Scholar
  55. 55.
    Schütte UME, Abdo Z, Foster J, Ravel J, Bunge J, Solheim B, Forney LJ (2010) Bacterial diversity in a glacier foreland of the high Arctic. Mol Ecol 19:54–66. doi:10.1111/j.1365-294X.2009.04479.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Laura C. Kelly
    • 1
    • 5
  • Charles S. Cockell
    • 1
    • 6
  • Thorsteinn Thorsteinsson
    • 2
  • Viggó Marteinsson
    • 3
  • John Stevenson
    • 4
  1. 1.Geomicrobiology Research Group, CEPSAROpen UniversityMilon KeynesUK
  2. 2.Hydrology DivisionNational Energy AuthorityReykjavikIceland
  3. 3.Matís Idt./Food SafetyEnvironment & GeneticsReykjavikIceland
  4. 4.School of GeosciencesUniversity of EdinburghEdinburghUK
  5. 5.School of Biology and Conservation EcologyManchester Metropolitan UniversityManchesterUK
  6. 6.School of Physics and AstronomyUniversity of EdinburghEdinburghUK

Personalised recommendations