Microbial Ecology

, Volume 71, Issue 1, pp 18–28 | Cite as

Effects of Volcanic Pumice Inputs on Microbial Community Composition and Dissolved C/P Ratios in Lake Waters: an Experimental Approach

  • B. E. Modenutti
  • E. G. Balseiro
  • M. A. Bastidas Navarro
  • Z. M. Lee
  • M. S. Souza
  • J. R. Corman
  • J. J. Elser
Microbiology of Aquatic Systems

Abstract

Volcanic eruptions discharge massive amounts of ash and pumice that decrease light penetration in lakes and lead to concomitant increases in phosphorus (P) concentrations and shifts in soluble C/P ratios. The consequences of these sudden changes for bacteria community composition, metabolism, and enzymatic activity remain unclear, especially for the dynamic period immediately after pumice deposition. Thus, the main aim of our study was to determine how ambient bacterial communities respond to pumice inputs in lakes that differ in dissolved organic carbon (DOC) and P concentrations and to what extent these responses are moderated by substrate C/P stoichiometry. We performed an outdoor experiment with natural lake water from two lakes that differed in dissolved organic carbon (DOC) concentration. We measured nutrient concentrations, alkaline phosphatase activity (APA), and DOC consumption rates and assessed different components of bacterial community structure using next-generation sequencing of the 16S rRNA gene. Pumice inputs caused a decrease in the C/P ratio of dissolved resources, a decrease in APA, and an increase in DOC consumption, indicating reduced P limitation. These changes in bacteria metabolism were coupled with modifications in the assemblage composition and an increase in diversity, with increases in bacterial taxa associated with biofilm and sediments, in predatory bacteria, and in bacteria with gliding motility. Our results confirm that volcanic eruptions have the potential to alter nutrient partitioning and light penetration in receiving waterways which can have dramatic impacts on microbial community dynamics.

Keywords

Eruption Bacteria diversity Dissolved resources 

Notes

Acknowledgments

This work was supported by the Fondo Para la Investigación Científica y Tecnológica Argentina [FONCyT PICT2240, PICT1168, PICT0929], the CONICET-NSF Cooperation Program, the US National Science Foundation, the NASA Astrobiology Institute, and the National Geographic Society [NGS9005/11]. J.J.E. acknowledges support from the Fulbright Foundation.

Supplementary material

248_2015_707_MOESM1_ESM.tif (40.9 mb)
High Resolution image (TIF 41920 kb)
248_2015_707_MOESM2_ESM.eps (92 kb)
High Resolution image (EPS 92 kb)
248_2015_707_MOESM3_ESM.eps (136 kb)
High Resolution image (EPS 135 kb)
248_2015_707_MOESM4_ESM.eps (116 kb)
High Resolution image (EPS 115 kb)
248_2015_707_MOESM5_ESM.eps (1.6 mb)
High Resolution image (EPS 1597 kb)
248_2015_707_MOESM6_ESM.eps (148 kb)
High Resolution image (EPS 148 kb)

References

  1. 1.
    APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, AWWA, Washington, DCGoogle Scholar
  2. 2.
    Arrieta JM, Herndl GI (2002) Changes in bacterial beta-glucosidase diversity during a coastal phytoplankton bloom. Limnol Oceanogr 47:594–599CrossRefGoogle Scholar
  3. 3.
    Bastidas Navarro M, Modenutti BE, Callieri C, Bertoni R, Balseiro EG (2009) Balance between primary and bacterial production in North Patagonian shallow lakes. Aquat Ecol 43:867–878CrossRefGoogle Scholar
  4. 4.
    Brasier MD, Matthewman R, McMahon S, Wacey D (2011) Pumice as a remarkable substrate for the origin of life. Astrobiology 11:725–734CrossRefPubMedGoogle Scholar
  5. 5.
    Caneiro A, Mogni L, Serquis A, Cotaro C, Wilberger D, Ayala C, Daga R, Poire D, Scerbo E (2011) Análisis de cenizas volcánicas del Cordón Caulle (complejo volcánico Puyehue-Cordón Caulle). Comisión Nacional de Energía Atómicahttp://cab.cnea.gov.ar/noticiasanteriores/erupcionCaulle2011/InformeCenizas.pdf
  6. 6.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Chrzanowski TH, Kyle M (1996) Ratios of carbon, nitrogen and phosphorus in Pseudomonas fluorescens as a model for bacterial element ratios and nutrient regeneration. Aquat Microb Ecol 10:115–122CrossRefGoogle Scholar
  8. 8.
    Dahl E, Bagøien E, Edvardsen B, Stenseth NC (2005) The dynamics of Chrysochromulina species in the Skagerrak in relation to environmental conditions. J Sea Res 54:15–24CrossRefGoogle Scholar
  9. 9.
    Del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541CrossRefGoogle Scholar
  10. 10.
    del Giorgio PA, Newell RE (2012) Phosphorus and DOC availability influence the partitioning between bacterioplankton production and respiration in tidal marsh ecosystems. Environ Microbiol 14:1296–1307CrossRefPubMedGoogle Scholar
  11. 11.
    Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366Google Scholar
  12. 12.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Edmondson W (1984) Volcanic ash in lakes. NW Environ J 1:139–150Google Scholar
  14. 14.
    Edmondson W, Litt AH (1984) Mount St Helens ash in lakes in the lower Grand Coulee, Washington State. Verh Int Verein Limnol 22:510–512Google Scholar
  15. 15.
    Einarsson A, Óskarsson H, Haflidason H (1993) Stratigraphy of fossil pigments and Cladophora and its relationship with deposition of tephra in Lake Mývatn, Iceland. J Paleolimnol 8:15–26Google Scholar
  16. 16.
    Elifantz H, Horn G, Ayon M, Cohen Y, Minz D (2013) Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater. FEMS Microbiol Ecol 85:348–357CrossRefPubMedGoogle Scholar
  17. 17.
    Elser JJ, Bastidas M, Corman JR, Emick H, Kellom M, Laspoumaderes C, Lee ZM, Poret-Peterson A, Balseiro E, Modenutti B (2015) Community structure and biogeochemical impacts of microbial life on floating pumice. Appl Environ Microbiol 81:1542–1549CrossRefPubMedCentralPubMedGoogle Scholar
  18. 18.
    Frogner P, Gíslason SR, Óskarsson N (2001) Fertilizing potential of volcanic ash in ocean surface water. Geology 29:487–490CrossRefGoogle Scholar
  19. 19.
    Gage M, Gorham E (1985) Alkaline phosphatase activity and cellular phosphorus as an index of the phosphorus status of phytoplankton in Minnesota lakes. Freshw Biol 15:227–233CrossRefGoogle Scholar
  20. 20.
    Godwin CM, Cotner JB (2014) Carbon:phosphorus homeostasis of aquatic bacterial assemblages is mediated by shifts in assemblage composition. Aquat Microb Ecol 73:245–258CrossRefGoogle Scholar
  21. 21.
    Godwin CM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J 9:2324–2347CrossRefPubMedGoogle Scholar
  22. 22.
    Guillemette F, del Giorgio PA (2011) Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems. Limnol Oceanogr 56:734–748CrossRefGoogle Scholar
  23. 23.
    Hamme RC, Webley PW, Crawford WR, Whitney FA, DeGrandpre MD, Emerson SR, Eriksen CC, Giesbrecht KE, Gower JFR, Kavanaugh MT, Peña MA, Sabine CL, Batten SD, Coogan LA, Grundle DS, Lockwood D (2010) Volcanic ash fuels anomalous plankton bloom in subarctic northeast Pacific. Geophys Res Lett 37:L19604. doi: 10.1029/2010GL044629 CrossRefGoogle Scholar
  24. 24.
    Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273CrossRefPubMedGoogle Scholar
  25. 25.
    Hoppe H-G (1993) Use of fluorogenic model substrates for extracellular enzyme activity (EEA) measurement of bacteria. Handbook of methods in aquatic microbial ecology. 423-431Google Scholar
  26. 26.
    Jansson M, Bergstrom AK, Lymer D, Vrede K, Karlsson J (2006) Bacterioplankton growth and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microb Ecol 52:358–364CrossRefPubMedGoogle Scholar
  27. 27.
    Labry C, Delmas D, Herbland A (2005) Phytoplankton and bacterial alkaline phosphatase activities in relation to phosphate and DOP availability within the Gironde plume waters (Bay of Biscay). J Exp Mar Biol Ecol 318:213–225CrossRefGoogle Scholar
  28. 28.
    Lennon JT, Pfaff LE (2005) Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquat Microb Ecol 39:107–119CrossRefGoogle Scholar
  29. 29.
    Lin II, Hu C, Li Y-H, Ho T-Y, Fischer TP, Wong GTF, Wu J, Huang C-W, Chu DA, Ko DS, Chen J-P (2011) Fertilization potential of volcanic dust in the low-nutrient low-chlorophyll western North Pacific subtropical gyre: Satellite evidence and laboratory study. Glob Biogeochem Cycles 25:GB1006. doi: 10.1029/2009GB003758 Google Scholar
  30. 30.
    McCallister SL, del Giorgio PA (2008) Direct measurement of the delta-13C signature of carbon respired by bacteria in lakes: linkages to potential carbon sources, ecosystem baseline metabolism, and CO2 fluxes. Limnol Oceanogr 53:1204–1216CrossRefGoogle Scholar
  31. 31.
    Modenutti BE, Balseiro EG, Bastidas Navarro M, Laspoumaderes C, Souza MS, Cuassolo F (2013) Environmental changes affecting light climate in oligotrophic mountain lakes: the deep chlorophyll maxima as a sensitive variable. Aquat Sci 75:361–371CrossRefGoogle Scholar
  32. 32.
    Modenutti BE, Balseiro EG, Elser JJ, Bastidas Navarro M, Cuassolo F, Laspoumaderes C, Souza MS, Dıaz Villanueva V (2013) Effect of volcanic eruption on nutrients, light, and phytoplankton in oligotrophic lakes. Limnol Oceanogr 58:1165–1175Google Scholar
  33. 33.
    Morris DP, Zagarese H, Williamson CE, Balseiro EG, Hargreaves BR, Modenutti BE, Moeller R, Queimaliños C (1995) The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol Oceanogr 40:1381–1391CrossRefGoogle Scholar
  34. 34.
    Neuenschwander SM, Pernthaler J, Posch T, Salcher MM (2015) Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. Environ Microbiol 17:781–795CrossRefPubMedGoogle Scholar
  35. 35.
    Nusch EA (1980) Comparison of different methods for chlorophyll and phaeopigment determination. Arch Hydrobiol Beih Ergeb Limnol 14:14–36Google Scholar
  36. 36.
    Poindexter JS (2006) Dimorphic prosthecate bacteria: the genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron. The prokaryotes. Springer, pp. 72-90Google Scholar
  37. 37.
    Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  38. 38.
    Rhee YJ, Han CR, Kim WC, Jun DY, Rhee IK, Kim YH (2010) Isolation of a novel freshwater agarolytic Cellvibrio sp. KY-YJ-3 and characterization of its extracellular beta-agarase. J Microbiol Biotechnol 20:1378–1385CrossRefPubMedGoogle Scholar
  39. 39.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Schwartz AW (2006) Phosphorus in prebiotic chemistry. Philos Trans R Soc B 361:1743–1749CrossRefGoogle Scholar
  41. 41.
    Self S (2006) The effects and consequences of very large explosive volcanic eruptions. Phil Trans R Soc A 364:2073–2097CrossRefPubMedGoogle Scholar
  42. 42.
    Sterner RW, Elser JJ, Fee EJ, Guildford SJ, Chrzanowski TH (1997) The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. Am Nat 150:663–684CrossRefPubMedGoogle Scholar
  43. 43.
    Team RCd (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  44. 44.
    Tittel J, Wiehle I, Wannicke N, Kampe H, Poerschmann J, Meier J, Kamjunke N (2009) Utilisation of terrestrial carbon by osmotrophic algae. Aquat Sci 71:46–54CrossRefGoogle Scholar
  45. 45.
    Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitt Internat Verein Limnol 9:38Google Scholar
  46. 46.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedCentralPubMedGoogle Scholar
  47. 47.
    Westrich JT, Berner RA (1984) The role of sedimentary organic matter in bacterial sulfate reduction: the G model tested. Limnol Oceanogr 29:236–249CrossRefGoogle Scholar
  48. 48.
    Williams HN, Lymperopoulou DS, Athar R, Chauhan A, Dickerson TL, Chen H, Laws E, Berhane TK, Flowers AR, Bradley N, Young S, Blackwood D, Murray J, Mustapha O, Blackwell C, Tung Y, Noble RT (2015) Halobacteriovorax, an underestimated predator on bacteria: potential impact relative to viruses on bacterial mortality. ISME J. doi: 10.1038/ismej.2015.129 PubMedCentralGoogle Scholar
  49. 49.
    Wissmar RC, Devol AH, Staley JT, Sedell JR (1982) Biological responses of lakes in the Mount St. Helens Blast Zone Sci 216:178–181Google Scholar
  50. 50.
    Yamagata Y, Watanabe H, Saitoh M, Namba T (1991) Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature 352:516–519CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • B. E. Modenutti
    • 1
  • E. G. Balseiro
    • 1
  • M. A. Bastidas Navarro
    • 1
  • Z. M. Lee
    • 2
  • M. S. Souza
    • 1
  • J. R. Corman
    • 2
    • 3
  • J. J. Elser
    • 2
  1. 1.Laboratorio de LimnologíaINIBIOMA, CONICET-University of ComahueBarilocheArgentina
  2. 2.School of Life SciencesArizona State UniversityTempeUSA
  3. 3.Center for LimnologyUniversity of Wisconsin-MadisonMadisonUSA

Personalised recommendations