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Extremophiles

, Volume 23, Issue 2, pp 249–263 | Cite as

The bacterial diversity on steam vents from Paricutín and Sapichu volcanoes

  • Elcia Margareth Souza BritoEmail author
  • Víctor Manuel Romero-Núñez
  • César Augusto Caretta
  • Pierre Bertin
  • Julio César Valerdi-Negreros
  • Rémy Guyoneaud
  • Marisol Goñi-Urriza
Original Paper

Abstract

Vapor steam vents are prevailing structures on geothermal sites in which local geochemical conditions allow the development of extremophilic microorganisms. We describe the structure of the prokaryotic community able to grow on the walls and rocks of such microecosystems in two terrestrial Mexican volcanoes: Paricutín (PI and PII samples) and its satellite Sapichu (S sample). The investigated samples showed similar diversity indices, with few dominant OTUs (abundance > 1%): 21, 16 and 23, respectively for PI, PII and S. However, each steam vent showed a particular community profile: PI was dominated by photosynthetic bacteria (Cyanobacteria and Chloroflexia class), PII by Actinobacteria and Proteobacteria, and S by Ktedonobacteria class, Acidobacteria and Cyanobacteria phyla. Concerning the predicted metabolic potential, we found a dominance of cellular pathways, especially the ones for energy generation with metabolisms for sulfur respiration, nitrogen fixation, methanogenesis, carbon fixation, photosynthesis, and metals, among others. We suggest a different maturity stage for the three studied fumaroles, from the youngest (PI) to the oldest (S and PII), also influenced by the temperature and other geochemical parameters. Furthermore, four anaerobic strains were isolated, belonging to Clostridia class (Clostridium sphenoides, C. swellfunanium and Anaerocolumna cellulosilytica) and to Bacilli class (Paenibacillus azoreducens).

Keywords

Extreme environment Volcanic fumaroles Anaerobic bacteria Microbial biodiversity Predictive metagenomics profiling 

Notes

Acknowledgements

This work was financially supported by BIOMETAL project (ANR-CONACyT-188775). We acknowledge the Direción de Apoyo a la Investigación y al Posgrado of Guanajuato University (DAIP) for a scholarship to Víctor Manuel Romero-Nuñez (Convocatoria Institucional de Investigación Científica, 627/2015). We are also grateful to Dra. L. M. Muñoz del Cote for kindly revising the written English of the manuscript, to Dr. B. Wemheuer for the help with Tax4Fun2 and to the anonymous referees for useful suggestions that improved the original version of the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

792_2019_1078_MOESM1_ESM.eps (1.7 mb)
Online Resource 1: Veen diagram for the OTUs data. The circle diameter represents the relative abundance of each sample (S, PI and PII)
792_2019_1078_MOESM2_ESM.eps (95 kb)
Online Resource 2: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to C-fixation pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM3_ESM.eps (83 kb)
Online Resource 3: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to other C-fixation pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM4_ESM.eps (97 kb)
Online Resource 4: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to photosynthesis pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM5_ESM.eps (95 kb)
Online Resource 5: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to methane metabolism pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM6_ESM.eps (92 kb)
Online Resource 6: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to N-fixation/oxido-reduction pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM7_ESM.eps (97 kb)
Online Resource 7: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to S-respiration pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM8_ESM.eps (98 kb)
Online Resource 8: Similar to Fig. 6, heatmap showing the predicted abundance of KO’s related to oligo-elements pathways. The color intensity marks the abundances according to the scale indicated on the top left side of the figure
792_2019_1078_MOESM9_ESM.eps (118 kb)
Online Resource 9: Phylogenetic tree based on 16S rRNA encode gene, showing the position of isolated strains within the radius of members of representative groups (Firmicute phylum). The tree was generated using maximum parsimony and neighbor-joining analysis. All accession numbers are indicated inside parenthesis

References

  1. Amaral A, Cruz J, Cunha RT, Rodrigues A (2006) Baseline levels of metals in volcanic soils of the Azores (Portugal). Soil Sediment Contam 15:123–130CrossRefGoogle Scholar
  2. Barton LL (2005) Physiological basis for growth in extreme environments. Structural and functional relationships in prokaryotes. Springer, New York, pp 348–393Google Scholar
  3. Benson CA, Bizzoco RW, Lipson DA, Kelley ST (2011) Microbial diversity in nonsulfur, sulfur and iron geothermal steam vents. FEMS Microbiol Ecol 76:74–88CrossRefGoogle Scholar
  4. Bhowmick D, Bal B, Chatterjee N, Ghosh A, Pal S (2009) A low-GC gram-positive Thermoanaerobacter-like bacterium isolated from an Indian hot spring contains Cr(VI) reduction activity both in the membrane and cytoplasm. J Appl Microbiol 106:2006–2016CrossRefGoogle Scholar
  5. Bioinformatics (2016) FastQC: a quality control tool for high throughput sequence data. Babraham Bioinformatics Institute, Cambridge, UK. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 01 February 2016
  6. Brito EMS, Piñón-Castillo HA, Guyoneaud R, Caretta CA, Gutiérrez-Corona JF, Duran R, Reyna-López GE, Nevárez-Moorillón GV, Fahy A, Goñi-Urriza M (2013) Bacterial biodiversity from anthropogenic extreme environments: a hyper-alkaline and hyper-saline industrial residue contaminated by chromium and iron. Appl Microbiol Biot 97:369–378CrossRefGoogle Scholar
  7. Brito EMS, Villegas-Negrete N, Sotelo-González IA, Caretta CA, Goñi-Urriza M, Gassie C, Hakil F, Colin Y, Duran R, Gutiérrez-Corona F, Piñón-Castillo HA, Cuevas-Rodríguez G, Malm O, Torres JPM, Fahy A, Reyna-López GE, Guyoneaud R (2014) Microbial diversity in Los Azufres geothermal field (Michoacán, Mexico) and isolation of representative sulfate and sulfur reducers. Extremophiles 18:385–398CrossRefGoogle Scholar
  8. Cavaletti L, Monciardini P, Bamonte R, Schumann P, Rohde M, Sosio M, Donadio S (2006) New lineage of filamentous, spore- forming, Gram-positive bacteria from soil. Appl Environ Microbiol 72:4360–4369CrossRefGoogle Scholar
  9. Cebriá J, Martiny B, López-Ruiz J, Morán-Zenteno D (2011) The Parícutin calc-alkaline lavas: new geochemical and petrogenetic modelling constraints on the crustal assimilation process. J Volcanol Geotherm Res 201:113–125CrossRefGoogle Scholar
  10. Cockell C, Olsson-francis K, Herrera A, Meunier A (2009) Alteration textures in terrestrial volcanic glass and the associated bacterial community. Geobiology 7:50–65CrossRefGoogle Scholar
  11. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310CrossRefGoogle Scholar
  12. Cortés-Palomec AC, McCauley RA, Oyama K (2008) Isolation, characterization and cross-amplification of polymorphic microsatellite loci in Laelia speciosa (orchidaceae). Mol Ecol Res 8:135–138CrossRefGoogle Scholar
  13. Costello EK, Halloy SR, Reed SC, Sowell P, Schmidt SK (2009) Fumarole-supported islands of biodiversity within a hyperarid, high-elevation landscape on Socompa volcano, Puna de Atacama, Andes. Appl Environ Microbiol 75:735–747CrossRefGoogle Scholar
  14. Crossey LJ, Karlstrom KE, Schmandt B, Crow RR, Colman DR, Cron B, Takacs-Vesbach CD, Dahm CN, Northup DE, Hilton DR, Jason WR, Lowry AR (2016) Continental smokers couple mantle degassing and distinctive microbiology within continents. Earth Planet Sci Lett 435:22–30CrossRefGoogle Scholar
  15. Cuecas A, Portillo M, Kanoksilapatham W, Gonzalez J (2014) Bacterial distribution along a 50°C temperature gradient reveals a parceled out hot spring environment. Microbial Ecol 68:729–739CrossRefGoogle Scholar
  16. Delfosse T, Delmelle P, Iserentant A, Delvaux B (2003) Heavy metal concentrations in soils downwind from Masaya volcano (Nicaragua). In: Americal Geophysical Union, Fall Meeting Abstracts, V1-0525Google Scholar
  17. Edgar RC (2010) Search and clustering orders of magnitude faster than blast. Bioinformatics 26:2460–2461CrossRefGoogle Scholar
  18. Fierros-Romero G, Gómez-Ramírez M, Arenas-Isaac GE, Pless RC, Rojas-Avelizapa NG (2016) Identification of Bacillus megaterium and Microbacterium liquefaciens genes involved in metal resistance and metal removal. Can J Microbiol 62:505–513CrossRefGoogle Scholar
  19. Fierros-Romero G, Wrosek-Cabrera JA, Gómez-Ramírez M, Pless RC, Rivas-Castillo A, Rojas-Avelizapa NG (2017) Expression changes in metal-resistance genes in Microbacterium liquefaciens under nickel and vanadium exposure. Curr Microbiol 74:840–847CrossRefGoogle Scholar
  20. Fude L, Harris B, Urrutia MM, Beveridge TJ (1994) Reduction of Cr(VI) by a consortium of sulfate-reducing bacteria (SRB III). Appl Environ Microbiol 60:1525–1531Google Scholar
  21. Gardine M, West ME, Cox T (2011) Dike emplacement near Parícutin volcano, Mexico in 2006. Bull Volcanol 73:123–132CrossRefGoogle Scholar
  22. Gómez-Ramírez M, Montero-Álvarez LA, Tobón-Avilés A, Fierros-Romero G, Rojas-Avelizapa NG (2015) Microbacterium oxydans and Microbacterium liquefaciens: a biological alternative for the treatment of Ni-V-containing wastes. J Environ Sci Health Part A 50:602–610Google Scholar
  23. Hasenaka T, Carmichael IS (1985) The cinder cones of Michoacán-Guanajuato, central Mexico: their age, volume and distribution, and magma discharge rate. J Volcanol Geotherm Res 25:105–124CrossRefGoogle Scholar
  24. Hedlund BP, Dodsworth JA, Murugapiran SK, Rinke C, Woyke T (2014) Impact of single-cell genomics and metagenomics on the emerging view of extremophile “microbial dark matter”. Extremophiles 18:865–875CrossRefGoogle Scholar
  25. Hong C, Si Y, Xing Y, Li Y (2015) Illumina miseq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environ Sci Pollut Res 22:10788–10799CrossRefGoogle Scholar
  26. Huang Q, Dong CZ, Dong RM, Jiang H, Wang S, Wang G, Fang B, Ding X, Niu L, Li X, Zhang C, Dong H (2011) Archaeal and bacterial diversity in hot springs on the Tibetan plateau, China. Extremophiles 15:549–563CrossRefGoogle Scholar
  27. Hungate R (1969) A roll tube method for cultivation of strict anaerobes. In: Methods in microbiology, Academic Press, London, pp 117–132Google Scholar
  28. Inskeep WP, Jay ZJ, Tringe SG, Herrgard M, Rusch DB (2013) The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front Microbiol 4:1–15Google Scholar
  29. Katoh K, Standley DM (2013) Mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780CrossRefGoogle Scholar
  30. Kelly LC, Cockell CS, Piceno YM, Andersen GL, Thorsteinsson T, Marteinsson V (2010) Bacterial diversity of weathered terrestrial Icelandic volcanic glasses. Microbial Ecol 60:740–752CrossRefGoogle Scholar
  31. Kelly LC, Cockell CS, Herrera-Belaroussi A, Piceno Y, Andersen G, DeSantis T, Brodie E, Thorsteinsson T, Marteinsson V, Poly F, LeRoux X (2011) Bacterial diversity of terrestrial crystalline volcanic rocks, Iceland. Microbial Ecol 62:69–79CrossRefGoogle Scholar
  32. Kelly LC, Cockell CS, Thorsteinsson T, Marteinsson V, Stevenson J (2014) Pioneer microbial communities of the Fimmvörðuháls lava flow, Eyjafjallajökull, Iceland. Microbial Ecol 68:504–518CrossRefGoogle Scholar
  33. Krauskopf KB (1948) Mechanism of eruption at Paricutín Volcano, Mexico. Geol Soc Am Bull 59(8):711–731CrossRefGoogle Scholar
  34. Lane D (1991) 16S/23S rRNA sequencing. In: Nucleic acid techniques in bacterial systematics, Wiley, Chichester, pp 125–175Google Scholar
  35. Liu C, Huang D, Liu L, Zhang J, Deng Y, Chen L, Zhang W, Wu Z, Fan A, Lai D, Dai L (2014) Clostridium swellfunianum sp. nov., a novel anaerobic bacterium isolated from the pit mud of chinese luzhou-flavor liquor production. Antonie Van Leeuwenhoek 106:817–825CrossRefGoogle Scholar
  36. Mayhew LE, Geist DJ, Childers SE, Pierson JD (2007) Microbial community comparisons as a function of the physical and geo-chemical conditions of Galápagos island fumaroles. Geomicrobiol J 24:615–625CrossRefGoogle Scholar
  37. Medrano-Santillana M, Brito EMS, Duran R, Gutiérrez-Corona F, Reyna-López GE (2017) Bacterial diversity in fumarole environments of the Paricutín volcano, Michoacán (Mexico). Extremophiles 21:499–511CrossRefGoogle Scholar
  38. Meehan C, Bjourson AJ, McMullan G (2001) Paenibacillus azoreducens sp. nov., a synthetic azo dye decolorizing bacterium from industrial wastewater. Int J Syst Evol Microbiol 51:1681–1685CrossRefGoogle Scholar
  39. Miller SR, Strong AL, Jones KL, Ungerer MC (2009) Bar-coded pyrosequencing reveals shared bacterial community properties along the temperature gradients of two alkaline hot springs in Yellowstone National Park. Appl Environ Microbiol 75:4565–4572CrossRefGoogle Scholar
  40. Oberauner L, Zachow C, Lackner S, Högenauer C, Smolle K-H, Berg G (2013) The ignored diversity: complex bacterial communities in intensive care units revealed by 16S pyrosequencing. Sci Rep 3:1413–1424CrossRefGoogle Scholar
  41. Overmann J, Fischer U, Pfennig N (1992) A new purple sulfur bacterium from saline littoral sediments, Thiorhodovibrio winogradskyi gen. nov. and sp. nov. Arch Microbiol 157:329–335CrossRefGoogle Scholar
  42. Pattanapipitpaisal P, Brown N, Macaskie L (2001) Chromate reduction by Microbacterium liquefaciens immobilised in polyvinyl alcohol. Biotechnol Lett 23:61–65CrossRefGoogle Scholar
  43. Rosa M, Gambacorta A, Bu’Lock JD (1975) Extremely thermophilic acidophilic bacteria convergent with Sulfolobus acidocaldarius. Microbiology 86:156–164Google Scholar
  44. Rudi K, Skulberg OM, Larsen F, Jakobsen KS (1997) Strain characterization and classification of oxyphotobacteria in clone cultures on the basis of 16S rRNA sequences from the variable regions V6, V7, and V8. Appl Environ Microbiol 63:2593–2599Google Scholar
  45. Satchanska G, Selenska-Pobell S (2005) Bacterial diversity in the uranium mill-tailing gittersee as estimated via a 16S rDNA approach. Comptes rendus Acad bulgar Sci 58:1105–1112Google Scholar
  46. Stott MB, Crowe MA, Mountain BW, Smirnova AV, Hou S, Alam M, Dunfield PF (2008) Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ Microbiol 10:2030–2041CrossRefGoogle Scholar
  47. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) Mega6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  48. Tomova I, Stoilova-Disheva M, Lyutskanova D, Pascual J, Petrov P, Kambourova M (2010) Phylogenetic analysis of the bacterial community in a geothermal spring, rupi basin, Bulgaria. World J Microbiol Biotechnol 26:2019–2028CrossRefGoogle Scholar
  49. Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338CrossRefGoogle Scholar
  50. Ueki A, Ohtaki Y, Kaku N, Ueki K (2016) Descriptions of Anaerotaenia torta gen. nov., sp. nov. and Anaerocolumna cellulosilytica gen. nov., sp. nov. isolated from a methanogenic reactor of cattle waste and reclassification of Clostridium aminovalericum, Clostridium jejuense and Clostridium xylanovorans as Anaerocolumna species. Int J Syst Evol Microbiol 66:2936–2943CrossRefGoogle Scholar
  51. Wall K, Cornell J, Bizzoco RW, Kelley ST (2015) Biodiversity hot spot on a hot spot: novel extremophile diversity in hawaiian fumaroles. Microbiol Open 4:267–281CrossRefGoogle Scholar
  52. Wang S, Hou W, Dong H, Jiang H, Huang L, Wu G, Zhang C, Song Z, Zhang Y, Ren H, Zhang J, Zhang L (2013) Control of temperature on microbial community structure in hot springs of the tibetan plateau. PLoS One 8:e62901CrossRefGoogle Scholar
  53. Wemheuer B (2018) Predicting functional profiles from metagenomic 16S rRNA data. Source Forge. http://sourceforge.net/p/tax4fun2/wiki/Home/. Accessed 29 August 2018
  54. Widdel F, Bak F (1992) Gram-negative mesophilic sulfate- reducing bacteria. In: Baloea A, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer, New York, pp 3352–3378CrossRefGoogle Scholar
  55. Yabe S, Aiba Y, Sakai Y, Hazaka M, Yokota A et al (2010) Thermosporothrix hazakensis gen. nov., sp. nov., isolated from compost, description of thermosporotrichaceae fam. nov. within the class ktedonobacteria cavaletti et al. 2007 and emended description of the class ktedonobacteria. Int J Syst Evol Microbiol 60:1794–1801CrossRefGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Ingeniería Ambiental, División de Ingenierías (CGT)Universidad de GuanajuatoGuanajuatoMexico
  2. 2.Departamento de Astronomía, División de Ciencias Naturales y Exactas (CGT)Universidad de GuanajuatoGuanajuatoMexico
  3. 3.Equipe Génomique, Structure et Traduction, Inst. Biologie Intégrative de la Cellule (I2BC) CNRS-UMR9198Universitè Paris-SudOrsay CedexFrance
  4. 4.CNRS/Universitè de Pau et des Pays de l’Adour/E2S, Institut des Sciences Analytiques et de Physicochimie pour l‘Environnement et les Matériaux, Environmental Microbiology Group, UMR 5254PauFrance

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