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

  • Microbiology of Aquatic Systems
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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.

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References

  1. APHA (2005) Standard methods for the examination of water and wastewater. American Public Health Association, AWWA, Washington, DC

    Google Scholar 

  2. Arrieta JM, Herndl GI (2002) Changes in bacterial beta-glucosidase diversity during a coastal phytoplankton bloom. Limnol Oceanogr 47:594–599

    Article  CAS  Google Scholar 

  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 43:867–878

    Article  Google Scholar 

  4. Brasier MD, Matthewman R, McMahon S, Wacey D (2011) Pumice as a remarkable substrate for the origin of life. Astrobiology 11:725–734

    Article  PubMed  CAS  Google Scholar 

  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. 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 6:1621–1624

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  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 10:115–122

    Article  Google Scholar 

  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 54:15–24

    Article  Google Scholar 

  9. Del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29:503–541

    Article  Google Scholar 

  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 14:1296–1307

    Article  PubMed  Google Scholar 

  11. Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  12. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  13. Edmondson W (1984) Volcanic ash in lakes. NW Environ J 1:139–150

    Google Scholar 

  14. Edmondson W, Litt AH (1984) Mount St Helens ash in lakes in the lower Grand Coulee, Washington State. Verh Int Verein Limnol 22:510–512

    Google Scholar 

  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 8:15–26

    Google Scholar 

  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 85:348–357

    Article  PubMed  CAS  Google Scholar 

  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 81:1542–1549

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  18. Frogner P, Gíslason SR, Óskarsson N (2001) Fertilizing potential of volcanic ash in ocean surface water. Geology 29:487–490

    Article  CAS  Google Scholar 

  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 15:227–233

    Article  CAS  Google Scholar 

  20. Godwin CM, Cotner JB (2014) Carbon:phosphorus homeostasis of aquatic bacterial assemblages is mediated by shifts in assemblage composition. Aquat Microb Ecol 73:245–258

    Article  Google Scholar 

  21. Godwin CM, Cotner JB (2015) Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J 9:2324–2347

    Article  PubMed  CAS  Google Scholar 

  22. Guillemette F, del Giorgio PA (2011) Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems. Limnol Oceanogr 56:734–748

    Article  CAS  Google Scholar 

  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

    Article  Google Scholar 

  24. Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273

    Article  PubMed  CAS  Google Scholar 

  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. 423-431

  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 52:358–364

    Article  PubMed  CAS  Google Scholar 

  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 318:213–225

    Article  CAS  Google Scholar 

  28. Lennon JT, Pfaff LE (2005) Source and supply of terrestrial organic matter affects aquatic microbial metabolism. Aquat Microb Ecol 39:107–119

    Article  Google Scholar 

  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. 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 53:1204–1216

    Article  CAS  Google Scholar 

  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 75:361–371

    Article  CAS  Google Scholar 

  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 58:1165–1175

    Google Scholar 

  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 40:1381–1391

    Article  CAS  Google Scholar 

  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 17:781–795

    Article  PubMed  CAS  Google Scholar 

  35. Nusch EA (1980) Comparison of different methods for chlorophyll and phaeopigment determination. Arch Hydrobiol Beih Ergeb Limnol 14:14–36

    CAS  Google Scholar 

  36. Poindexter JS (2006) Dimorphic prosthecate bacteria: the genera Caulobacter, Asticcacaulis, Hyphomicrobium, Pedomicrobium, Hyphomonas and Thiodendron. The prokaryotes. Springer, pp. 72-90

  37. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  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 20:1378–1385

    Article  PubMed  CAS  Google Scholar 

  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 75:7537–7541

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  40. Schwartz AW (2006) Phosphorus in prebiotic chemistry. Philos Trans R Soc B 361:1743–1749

    Article  CAS  Google Scholar 

  41. Self S (2006) The effects and consequences of very large explosive volcanic eruptions. Phil Trans R Soc A 364:2073–2097

    Article  PubMed  CAS  Google Scholar 

  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 150:663–684

    Article  PubMed  CAS  Google Scholar 

  43. Team RCd (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  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 71:46–54

    Article  CAS  Google Scholar 

  45. Utermöhl H (1958) Zur vervollkommnung der quantitativen phytoplankton-methodik. Mitt Internat Verein Limnol 9:38

    Google Scholar 

  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 73:5261–5267

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  47. Westrich JT, Berner RA (1984) The role of sedimentary organic matter in bacterial sulfate reduction: the G model tested. Limnol Oceanogr 29:236–249

    Article  CAS  Google Scholar 

  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

    PubMed Central  Google Scholar 

  49. Wissmar RC, Devol AH, Staley JT, Sedell JR (1982) Biological responses of lakes in the Mount St. Helens Blast Zone Sci 216:178–181

    CAS  Google Scholar 

  50. Yamagata Y, Watanabe H, Saitoh M, Namba T (1991) Volcanic production of polyphosphates and its relevance to prebiotic evolution. Nature 352:516–519

    Article  PubMed  CAS  Google Scholar 

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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.

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Correspondence to B. E. Modenutti.

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Fig. S1

Photographs of two lakes (a-Piré and b-Los Patos) covered with volcanic pumice during the Puyehue Cordón Caulle eruption. (GIF 1685 kb)

High Resolution image (TIF 41920 kb)

Fig. S2

Dissolved inorganic nitrogen (DIN) at the end of the experiment (T 15). (GIF 20 kb)

High Resolution image (EPS 92 kb)

Fig. S3

Dynamics of the abundance of mixotrophic (MxNF) and heterotrophic (HNF) nanoflagellates in the different treatments. a: MxNF Lake Escondido, b: MxNF Lake Gutiérrez, c: HNF Lake Escondido, d: HNF Lake Gutiérrez. (GIF 33 kb)

High Resolution image (EPS 135 kb)

Fig. S4

Total bacterial abundances in the different treatments during the experiment. (GIF 11 kb)

High Resolution image (EPS 115 kb)

Fig. S5

Bacterial community structure at the start of the experiment (T 0). (GIF 38 kb)

High Resolution image (EPS 1597 kb)

Fig. S6

Rank-abundance curve for the 100 most abundant genera in each treatment. The y-axis is represented as average percent relative abundance. Please note the change in scale. (GIF 24 kb)

High Resolution image (EPS 148 kb)

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Modenutti, B.E., Balseiro, E.G., Bastidas Navarro, M.A. et al. Effects of Volcanic Pumice Inputs on Microbial Community Composition and Dissolved C/P Ratios in Lake Waters: an Experimental Approach. Microb Ecol 71, 18–28 (2016). https://doi.org/10.1007/s00248-015-0707-3

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  • DOI: https://doi.org/10.1007/s00248-015-0707-3

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