Table of Contents Author Guidelines Submit a Manuscript
Archaea
Volume 2015, Article ID 646820, 11 pages
http://dx.doi.org/10.1155/2015/646820
Research Article

Archaeal Communities in a Heterogeneous Hypersaline-Alkaline Soil

1Cátedras CONACYT, Centro de Investigación en Ciencias Biológicas, Universidad Autónoma de Tlaxcala, Km. 10.5 Autopista Tlaxcala-Texmelucan, 90120 San Felipe Ixtacuixtla, TLAX, Mexico
2Laboratory of Soil Ecology, ABACUS, Cinvestav, Avenida Instituto Politécnico Nacional 2508, 07360 Mexico City, DF, Mexico

Received 1 February 2015; Accepted 15 April 2015

Academic Editor: Antonio Ventosa

Copyright © 2015 Yendi E. Navarro-Noya et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A.-Ş. Andrei, H. L. Banciu, and A. Oren, “Living with salt: metabolic and phylogenetic diversity of archaea inhabiting saline ecosystems,” FEMS Microbiology Letters, vol. 330, no. 1, pp. 1–9, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. J.-C. Auguet, A. Barberan, and E. O. Casamayor, “Global ecological patterns in uncultured Archaea,” The ISME Journal, vol. 4, no. 2, pp. 182–190, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. S. T. Bates, D. Berg-Lyons, J. G. Caporaso, W. A. Walters, R. Knight, and N. Fierer, “Examining the global distribution of dominant archaeal populations in soil,” The ISME Journal, vol. 5, no. 5, pp. 908–917, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. D. K. Oline, S. K. Schmidt, and M. C. Grant, “Biogeography and landscape-scale diversity of the dominant Crenarchaeota of soil,” Microbial Ecology, vol. 52, no. 3, pp. 480–490, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Oren, “Bioenergetic aspects of halophilism,” Microbiology and Molecular Biology Reviews, vol. 63, no. 2, pp. 334–348, 1999. View at Google Scholar · View at Scopus
  6. N. Oueriaghli, V. Béjar, E. Quesada, and F. Martínez-Checa, “Molecular ecology techniques reveal both spatial and temporal variations in the diversity of archaeal communities within the athalassohaline environment of Rambla Salada, Spain,” Microbial Ecology, vol. 66, no. 2, pp. 297–311, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. N. H. Youssef, K. N. Ashlock-Savage, and M. S. Elshahed, “Phylogenetic diversities and community structure of members of the extremely halophilic Archaea (order Halobacteriales) in multiple saline sediment habitats,” Applied and Environmental Microbiology, vol. 78, no. 5, pp. 1332–1344, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. C. P. Antony, D. Kumaresan, S. Hunger, H. L. Drake, J. C. Murrell, and Y. S. Shouche, “Microbiology of Lonar Lake and other soda lakes,” The ISME Journal, vol. 7, no. 3, pp. 468–476, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. W. D. Grant and S. Heaphy, “Metagenomics and recovery of enzyme genes from alkaline saline environments,” Environmental Technology, vol. 31, no. 10, pp. 1135–1143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. S. B. Humayoun, N. Bano, and J. T. Hollibaugh, “Depth distribution of microbial diversity in mono lake, a meromictic soda lake in California,” Applied and Environmental Microbiology, vol. 69, no. 2, pp. 1030–1042, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. V. Nolla-Ardèvol, M. Strous, D. Y. Sorokin, A. Y. Merkel, and H. E. Tegetmeyer, “Activity and diversity of haloalkaliphilic methanogens in Central Asian soda lakes,” Journal of Biotechnology, vol. 161, no. 2, pp. 167–173, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Y. Sorokin and J. G. Kuenen, “Chemolithotrophic haloalkaliphiles from soda lakes,” FEMS Microbiology Ecology, vol. 52, no. 3, pp. 287–295, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. N. M. Mesbah and J. Wiegel, “Life under multiple extreme conditions: diversity and physiology of the Halophilic alkalithermophiles,” Applied and Environmental Microbiology, vol. 78, no. 12, pp. 4074–4082, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. B. E. Jones and W. D. Grant, “Microbial diversity and ecology of alkaline environments,” in Journey to Diverse Microbial Worlds, vol. 2 of Cellular Origin and Life in Extreme Habitats, pp. 177–190, Springer, Dordrecht, The Netherlands, 2000. View at Publisher · View at Google Scholar
  15. D. Oh, K. Porter, B. Russ, D. Burns, and M. Dyall-Smith, “Diversity of Haloquadratum and other haloarchaea in three, geographically distant, Australian saltern crystallizer ponds,” Extremophiles, vol. 14, no. 2, pp. 161–169, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. L. Dendooven, R. J. Alcántara-Hernández, C. Valenzuela-Encinas, M. Luna-Guido, F. Perez-Guevara, and R. Marsch, “Dynamics of carbon and nitrogen in an extreme alkaline saline soil: a review,” Soil Biology and Biochemistry, vol. 42, no. 6, pp. 865–877, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. FAO, “Salt-affected soils and their management,” Soils Bulletin 39, FAO, Rome, Italy, 1988. View at Google Scholar
  18. S. Tripathi, A. Chakraborty, K. Chakrabarti, and B. K. Bandyopadhyay, “Enzyme activities and microbial biomass in coastal soils of India,” Soil Biology and Biochemistry, vol. 39, no. 11, pp. 2840–2848, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Ruiz-Romero, M. D. L. A. Coutiño-Coutiño, C. Valenzuela-Encinas, M. P. López-Ramírez, R. Marsch, and L. Dendooven, “Texcoconibacillus texcoconensis gen. nov., sp. nov., alkalophilic and halotolerant bacteria isolated from soil of the former lake Texcoco (Mexico),” International Journal of Systematic and Evolutionary Microbiology, vol. 63, no. 9, pp. 3336–3341, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Ruiz-Romero, K. B. Sánchez-López, M. D. L. A. Coutiño-Coutiño et al., “Natronobacterium texcoconense sp. nov., a haloalkaliphilic archaeon isolated from soil of a former lake Texcoco (Mexico),” International Journal of Systematic and Evolutionary Microbiology, vol. 63, no. 11, Article ID 053629, pp. 4163–4166, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Ruiz-Romero, C. Valenzuela-Encinas, M. P. López-Ramírez, M. de los Angeles Coutiño-Coutiño, R. Marsch, and L. Dendooven, “Natronorubrum texcoconense sp. nov., a haloalkaliphilic archaeon isolated from soil of the former lake Texcoco (Mexico),” Archives of Microbiology, vol. 195, no. 2, pp. 145–151, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Valenzuela-Encinas, I. Neria-González, R. J. Alcántara-Hernández et al., “Phylogenetic analysis of the archaeal community in an alkaline-saline soil of the former lake Texcoco (Mexico),” Extremophiles, vol. 12, no. 2, pp. 247–254, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Valenzuela-Encinas, I. Neria-González, R. J. Alcántara-Hernández et al., “Changes in the bacterial populations of the highly alkaline saline soil of the former lake Texcoco (Mexico) following flooding,” Extremophiles, vol. 13, no. 4, pp. 609–621, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Valenzuela-Encinas, R. J. Alcántara-Hernández, I. Estrada-Alvarado, F. J. Z.-D. de la Serna, L. Dendooven, and R. Marsch, “The archaeal diversity and population in a drained alkaline saline soil of the former Lake Texcoco (Mexico),” Geomicrobiology Journal, vol. 29, no. 1, pp. 18–22, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Alazard, C. Badillo, M.-L. Fardeau et al., “Tindallia texcoconensis sp. nov., a new haloalkaliphilic bacterium isolated from lake Texcoco, Mexico,” Extremophiles, vol. 11, no. 1, pp. 33–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Jan-Roblero, X. Magos, C. Hernández-Rodríguez, S. Le Borgne, and L. Fernández, “Phylogenetic analysis of bacterial populations in waters of the former Texcoco Lake, Mexico,” Canadian Journal of Microbiology, vol. 50, no. 12, pp. 1049–1059, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. G. W. Thomas, “Soil pH and soil acidity,” in Methods of Soil Analysis: Chemical Methods Part 3, D. L. Sparks, Ed., pp. 475–490, Soil Science Society of America Inc., American Society of Agronomy Inc., Madison, Wis, USA, 1996. View at Google Scholar
  28. W. C. Dahnke and D. A. Whitney, “Measurement of soil salinity,” in Recommended Chemical Soil Test Procedures for the North Central Region, W. C. Dahnke, Ed., pp. 32–34, North Dakota Agricultural Experiment Station Bulletin 499, Fargo, ND, USA, 1988. View at Google Scholar
  29. M. Amato, “Determination of carbon 12C and 14C in plant and soil,” Soil Biology and Biochemistry, vol. 15, no. 5, pp. 611–612, 1983. View at Publisher · View at Google Scholar · View at Scopus
  30. J. M. Bremner, “Total nitrogen,” in Methods of Soil Analysis Chemical Methods Part 3, D. L. Sparks, Ed., pp. 1085–1122, Soil Science Society of America, American Society of Agronomy, Madison, Wis, USA, 1996. View at Google Scholar
  31. G. W. Gee and J. W. Bauder, “Particle size analysis,” in Methods of soil Analysis, Part 1: Physical and Mineralogical Methods, A. Klute, Ed., pp. 383–411, Soil Science Society of America, American Society of Agronomy, Madison, Wis, U.S.A, 1986. View at Google Scholar
  32. M. A. Dojka, P. Hugenholtz, S. K. Haack, and N. R. Pace, “Microbial diversity in a hydrocarbon- and chlorinated-solvent- contaminated aquifer undergoing intrinsic bioremediation,” Applied and Environmental Microbiology, vol. 64, no. 10, pp. 3869–3877, 1998. View at Google Scholar · View at Scopus
  33. G. C. Baker, J. J. Smith, and D. A. Cowan, “Review and re-analysis of domain-specific 16S primers,” Journal of Microbiological Methods, vol. 55, no. 3, pp. 541–555, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Reeder and R. Knight, “Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions,” Nature Methods, vol. 7, no. 9, pp. 668–669, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. B. J. Haas, D. Gevers, A. M. Earl et al., “Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons,” Genome Research, vol. 21, no. 3, pp. 494–504, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. Q. Wang, G. M. Garrity, J. M. Tiedje, and J. R. Cole, “Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy,” Applied and Environmental Microbiology, vol. 73, no. 16, pp. 5261–5267, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Shannon, A. Markiel, O. Ozier et al., “Cytoscape: a software environment for integrated models of biomolecular interaction networks,” Genome Research, vol. 13, no. 11, pp. 2498–2504, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. J. G. Caporaso, K. Bittinger, F. D. Bushman, T. Z. DeSantis, G. L. Andersen, and R. Knight, “PyNAST: a flexible tool for aligning sequences to a template alignment,” Bioinformatics, vol. 26, no. 2, pp. 266–267, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. G. Caporaso, J. Kuczynski, J. Stombaugh et al., “QIIME allows analysis of high-throughput community sequencing data,” Nature Methods, vol. 7, no. 5, pp. 335–336, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Ochsenreiter, D. Selezi, A. Quaiser, L. Bonch-Osmolovskaya, and C. Schleper, “Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR,” Environmental Microbiology, vol. 5, no. 9, pp. 787–797, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. C. Brochier-Armanet, B. Boussau, S. Gribaldo, and P. Forterre, “Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota,” Nature Reviews Microbiology, vol. 6, no. 3, pp. 245–252, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. C. A. Francis, J. M. Beman, and M. M. M. Kuypers, “New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation,” The ISME Journal, vol. 1, no. 1, pp. 19–27, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. J. M. Gasol, E. O. Casamayor, I. Joint et al., “Control of heterotrophic prokaryotic abundance and growth rate in hypersaline planktonic environments,” Aquatic Microbial Ecology, vol. 34, no. 2, pp. 193–206, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Tindall, H. Ross, and W. Grant, “Natronobacterium gen. nov. and Natronococcus gen. nov., two new genera of haloalkaliphilic archaebacteria,” Systematic and Applied Microbiology, vol. 5, no. 1, pp. 41–57, 1984. View at Publisher · View at Google Scholar
  45. K. J. Bowers and J. Wiegel, “Temperature and pH optima of extremely halophilic Archaea: a mini-review,” Extremophiles, vol. 15, no. 2, pp. 119–128, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Oren, “Microbial life at high salt concentrations: phylogenetic and metabolic diversity,” Saline Systems, vol. 4, no. 1, article 2, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. M. E. Rhodes, S. T. Fitz-Gibbon, A. Oren, and C. H. House, “Amino acid signatures of salinity on an environmental scale with a focus on the Dead Sea,” Environmental Microbiology, vol. 12, no. 9, pp. 2613–2623, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Mwirichia, S. Cousin, A. W. Muigai, H. I. Boga, and E. Stackebrandt, “Archaeal diversity in the Haloalkaline lake Elmenteita in kenya,” Current Microbiology, vol. 60, no. 1, pp. 47–52, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Pagaling, H. Wang, M. Venables et al., “Microbial biogeography of six salt lakes in Inner Mongolia, China, and a salt lake in Argentina,” Applied and Environmental Microbiology, vol. 75, no. 18, pp. 5750–5760, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. T. Sime-Ngando, S. Lucas, A. Robin et al., “Diversity of virus-host systems in hypersaline Lake Retba, Senegal,” Environmental Microbiology, vol. 13, no. 8, pp. 1956–1972, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. C. P. Antony, J. C. Murrell, and Y. S. Shouche, “Molecular diversity of methanogens and identification of Methanolobus sp. as active methylotrophic Archaea in Lonar crater lake sediments,” FEMS Microbiology Ecology, vol. 81, no. 1, pp. 43–51, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. N. M. Mesbah, S. H. Abou-El-Ela, and J. Wiegel, “Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt,” Microbial Ecology, vol. 54, no. 4, pp. 598–617, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. B. Ollivier, M.-L. Fardeau, J.-L. Cayol et al., “Methanocalculus halotolerans gen. nov., sp. nov., isolated from an oil–producing well,” International Journal of Systematic Bacteriology, vol. 48, no. 3, pp. 821–828, 1998. View at Publisher · View at Google Scholar · View at Scopus
  54. V. P. Surakasi, A. A. Wani, Y. S. Shouche, and D. R. Ranade, “Phylogenetic analysis of methanogenic enrichment cultures obtained from Lonar Lake in India: isolation of Methanocalculus sp. and Methanoculleus sp.,” Microbial Ecology, vol. 54, no. 4, pp. 697–704, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. T. N. Zhilina, D. G. Zavarzina, V. V. Kevbrin, and T. V. Kolganova, “Methanocalculus natronophilus sp. nov., a new alkaliphilic hydrogenotrophic methanogenic archaeon from a soda lake, and proposal of the new family Methanocalculaceae,” Microbiology, vol. 82, no. 6, pp. 698–706, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. D. Y. Sorokin, B. Abbas, M. Geleijnse, N. V. Pimenov, M. V. Sukhacheva, and M. C. van Loosdrecht, “Methanogenesis at extremely haloalkaline conditions in the soda lakes of Kulunda Steppe (Altai, Russia),” FEMS Microbiology Ecology, vol. 91, no. 4, 2015. View at Publisher · View at Google Scholar
  57. T. N. Zhilina, D. G. Zavarzina, J. Kuever, A. M. Lysenko, and G. A. Zavarzin, “Desulfonatronum cooperativum sp. nov., a novel hydrogenotrophic, alkaliphilic, sulfate-reducing bacterium, from a syntrophic culture growing on acetate,” International Journal of Systematic and Evolutionary Microbiology, vol. 55, no. 3, pp. 1001–1006, 2005. View at Publisher · View at Google Scholar · View at Scopus