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Extremophiles

, Volume 18, Issue 4, pp 733–743 | Cite as

Bacterial colonization of a fumigated alkaline saline soil

  • Juan M. Bello-López
  • Cristina A. Domínguez-Mendoza
  • Arit S. de León-Lorenzana
  • Laura Delgado-Balbuena
  • Yendi E. Navarro-Noya
  • Selene Gómez-Acata
  • Analine Rodríguez-Valentín
  • Victor M. Ruíz-Valdiviezo
  • Marco Luna-Guido
  • Nele Verhulst
  • Bram Govaerts
  • Luc Dendooven
Original Paper

Abstract

After chloroform fumigating an arable soil, the relative abundance of phylotypes belonging to only two phyla (Actinobacteria and Firmicutes) and two orders [Actinomycetales and Bacillales (mostly Bacillus)] increased in a subsequent aerobic incubation, while it decreased for a wide range of bacterial groups. It remained to be seen if similar bacterial groups were affected when an extreme alkaline saline soil was fumigated. Soil with electrolytic conductivity between 139 and 157 dS m−1, and pH 10.0 and 10.3 was fumigated and the bacterial community structure determined after 0, 1, 5 and 10 days by analysis of the 16S rRNA gene, while an unfumigated soil served as control. The relative abundance of the Firmicutes increased in the fumigated soil (52.8 %) compared to the unfumigated soil (34.2 %), while that of the Bacteroidetes decreased from 16.2 % in the unfumigated soil to 8.8 % in the fumigated soil. Fumigation increased the relative abundance of the genus Bacillus from 14.7 % in the unfumigated soil to 25.7 %. It was found that phylotypes belonging to the Firmicutes, mostly of the genus Bacillus, were dominant in colonizing the fumigated alkaline saline as found in the arable soil, while the relative abundance of a wide range of bacterial groups decreased.

Keywords

Alkaliphiles Systematics, ecology, phylogeny Biodiversity Ecology Halophile: ecology, biotechnology, phylogeny, genetics, taxonomy, enzymes Molecular biology 

Notes

Acknowledgments

This research was funded by Cinvestav and ‘Apoyo Especial para el Fortalecimiento de Doctorado PNPC 2013’ from ‘Consejo Nacional de Ciencia y Tecnología’ (CONACyT, Mexico). The authors thank ABACUS-CONACyT. Y. E. N.–N. received a postdoctoral grant from CONACyT and ABACUS and J. M. B.-L. from CONACyT. C. A. D.-M, A. S. D.-L, L. D.-B, S. G.-A. and V. M. R.-V received grant-aided support from CONACyT.

Supplementary material

792_2014_653_MOESM1_ESM.pdf (32 kb)
Fig. S1. Emission of CO2 (mg CO2-C kg−1 dry soil) from the unfumigated (■) and fumigated (□) alkaline saline Texcoco soil incubated aerobically at 25 ± 2 °C for 10 days. Bars are one ± STD (PDF 31 kb)
792_2014_653_MOESM2_ESM.pdf (164 kb)
Fig. S2. Principal coordinate analysis of UniFrac weighted distances of the bacterial communities in fumigated and unfumigated soil incubated aerobically for 10 days (PDF 163 kb)

References

  1. Acinas SG, Klepac-Ceraj V, Hunt DE, Pharino C, Ceraj I, Distel DL, Polz MF (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430:551–553PubMedCrossRefGoogle Scholar
  2. Beltrán-Hernández RI, Luna-Guido ML, Dendooven L (2007) Emission of carbon dioxide and dynamics of inorganic N in a gradient of alkaline saline soils of the former lake Texcoco. Appl Soil Ecol 35:390–403CrossRefGoogle Scholar
  3. Cano RJ, Borucki MK (1995) Revival and identification of bacterial spores in 25- to 40-million-year-old dominican amber. Science 268:1060–1064PubMedCrossRefGoogle Scholar
  4. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010a) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267PubMedCentralPubMedCrossRefGoogle Scholar
  5. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010b) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336PubMedCentralPubMedCrossRefGoogle Scholar
  6. Ceja-Navarro JA, Rivera-Orduña FN, Patiño-Zúñiga L, Vila-Sanjurjo A, Crossa J, Govaerts B, Dendooven L (2010) Phylogenetic and multivariate analyses to determine the effects of different tillage and residue management practices on soil bacterial communities. Appl Environ Microbiol 76:3685–3691PubMedCentralPubMedCrossRefGoogle Scholar
  7. Chang DH, Lee JB, Lee GH, Rhee MS, Lee H, Bae KS, Park DS, Kim BC (2013) Sunxiuqini adokdonensis sp nov., isolated from deep sub-seafloor sediment. J Microbiol 51:741–746PubMedCrossRefGoogle Scholar
  8. Cucurachi M, Busconi M, Marudelli M, Soffritti G, Fogher C (2013) Direct amplification of new cellulase genes from woodland soil purified DNA. Mol Biol Rep 40:4317–4325PubMedCrossRefGoogle Scholar
  9. de la Haba RR, Sánchez-Porro C, Marquez MC, Ventosa A (2011) Taxonomy of halophiles. In: Horikoshi K (ed) Extremophiles handbook, Springer, Berlin, pp 256–308Google Scholar
  10. Dendooven L, Alcantara-Hernández RJ, Valenzuela-Encinas C, Luna-Guido M, Perez-Guevara F, Marsch R (2010) Dynamics of carbon and nitrogen in an extreme alkaline saline soil: a review. Soil Biol Biochem 42:865–877CrossRefGoogle Scholar
  11. Domínguez-Mendoza CA, Bello-López JM, Navarro-Noya YE, de León-Lorenzana AS, Delgado-Balbuena L, Gómez-Acata S, Ruíz-Valdiviezo VM, Ramirez-Villanueva DA, Luna-Guido M, Dendooven L (2014) Bacterial community structure in fumigated soil. Soil Biol Biochem 73:122–129CrossRefGoogle Scholar
  12. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461PubMedCrossRefGoogle Scholar
  13. España M, Rasche F, Kandeler E, Brune T, Rodriguez B, Bending GD, Cadisch G (2011) Identification of active bacteria involved in decomposition of complex maize and soybean residues in a tropical Vertisol using 15N-DNA stable isotope probing. Pedobiologia 54:187–193CrossRefGoogle Scholar
  14. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedCrossRefGoogle Scholar
  15. García-Fraile P, Velázquez E, Mateos PF, Martínez-Molina E, Rivas R (2008) Cohnella phaseolisp. nov., isolated from root nodules of Phaseolus coccineus in Spain, and emended description of the genus Cohnella. Int J Syst Evol Micr 58:1855–1859CrossRefGoogle Scholar
  16. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methé B, De Santis TZ, The Human Microbiome Consortium, Petrosino JF, Knight R, Birren BW (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504PubMedCentralPubMedCrossRefGoogle Scholar
  17. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27PubMedCentralPubMedCrossRefGoogle Scholar
  18. He YM, Xie KZ, Huang X, Gu WJ, Zhang FB, Tang SH (2013) Evolution of microbial community diversity and enzymatic activity during composting. Res Microbiol 164:189–198PubMedCrossRefGoogle Scholar
  19. Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol R 63:735–750Google Scholar
  20. Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil. V. A method for measuring soil biomass. Soil Biol Biochem 8:209–213CrossRefGoogle Scholar
  21. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453PubMedCentralPubMedCrossRefGoogle Scholar
  22. Kemmitt SJ, Lanyon CV, Waite IS, Wen Q, Addiscott TM, Bird NRA, O’Donnell AG, Brookes PC (2008) Mineralization of native soil organic matter is not regulated by the size, activity or composition of the soil microbial biomass—a new perspective. Soil Biol Biochem 40:61–73CrossRefGoogle Scholar
  23. Keshri J, Mishra A, Jha B (2013) Microbial population index and community structure in saline–alkaline soil using gene targeted metagenomics. Microbiol Res 168:165–173PubMedCrossRefGoogle Scholar
  24. Kolter R, Siegele DA, Tormo A (1993) The stationary phase of the bacterial life cycle. Ann Rev Microbiol 47:855–874CrossRefGoogle Scholar
  25. Li K, Liu R, Zhang H, Yun J (2013) The diversity and abundance of bacteria and oxygenic phototrophs in saline biological desert crusts in Xinjiang, Northwest China. Microb Ecol 66:40–48PubMedCrossRefGoogle Scholar
  26. Luna-Guido ML, Beltrán-Hernández RI, Solis-Ceballos NA, Hernández-Chavez N, Mercado-García F, Olalde-Portugal V, Catt JA, Dendooven L (2000) Chemical and biological characteristics of alkaline saline soils from the former Lake Texcoco as affected by artificial drainage. Biol Fert Soils 32:102–108CrossRefGoogle Scholar
  27. Luna-Guido ML, Vega J, Ponce-Mendoza A, Hernández-Hernández H, Montes M-C, Dendooven L (2003) Mineralization of 14C-labelled maize in alkaline saline soils. Plant Soil 250:29–38CrossRefGoogle Scholar
  28. Martins LF, Antunes LP, Pascon RC, de Oliveira JCF, Digiampietri LA, Barbosa D, Peixoto BM, Vallim MA, Viana-Niero C, Ostroski EH, Telles GP, Dias Z, da Cruz JB, Juliano L, Verjovski-Almeida S, da Silva AM, Setubal JC (2013) Metagenomic analysis of a tropical composting operation at the São Paulo zoo park reveals diversity of biomass degradation functions and organisms. PLoS ONE 8:6CrossRefGoogle Scholar
  29. Mueller T, Joergensen RG, Meyer B (1992) Estimation of soil microbial biomass-C in the presence of living roots by fumigation extraction. Soil Biol Biochem 24:179–181CrossRefGoogle Scholar
  30. Naether A, Foesel BU, Naegele V, Wust PK, Weinert J, Bonkowski M, Alt F, Oelmann Y, Polle A, Lohaus G, Gockel S, Hemp A, Kalko EK, Linsenmair KE, Pfeiffer S, Renner S, Schoning I, Weisser WW, Wells K, Fischer M, Overmann J, Friedrich MW (2012) Environmental factors affect acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406PubMedCentralPubMedCrossRefGoogle Scholar
  31. Navarro-Noya YE, Gómez-Acata S, Montoya-Ciriaco N, Rojas-Valdez A, Suárez-Arriaga MC, Valenzuela-Encinas C, Jiménez-Bueno N, Verhulst N, Govaerts B, Dendooven L (2013) Relative impacts of tillage, residue management and crop-rotation on soil bacterial communities in a semi-arid agroecosystem. Soil Biol Biochem 65:86–95CrossRefGoogle Scholar
  32. Navarro-Noya YE, Jiménez-Aguilar A, Valenzuela-Encinas C, Alcántara-Hernández RJ, Ruíz-Valdiviezo VM, Ponce-Mendoza A, Luna-Guido L, Marsch R, Dendooven L (2014) Bacterial communities in soil undermoss and lichen-mosscrusts. Geomicrobiol J 31:152–160CrossRefGoogle Scholar
  33. Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol R 63:334–348Google Scholar
  34. Partanen P, Hultman J, Paulin L, Auvinen P, Romantschuk M (2010) Bacterial diversity at different stages of the composting process. BMC Microbiol 10:94PubMedCentralPubMedCrossRefGoogle Scholar
  35. Pathma J, Sakthivel N (2013) Molecular and functional characterization of bacteria isolated from straw and goat manure based vermicompost. Appl Soil Ecol 70:33–47CrossRefGoogle Scholar
  36. Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650PubMedCentralPubMedCrossRefGoogle Scholar
  37. Ramírez-Fuentes E, Ponce-Mendoza A, Luna-Guido ML, Van den Broeck E, Dendooven L (2002) Incorporation of glucose-14C and NH4+ in microbial biomass of alkaline saline soil. Biol Fertil Soils 36:269–275CrossRefGoogle Scholar
  38. Ridge EH (1976) Studies on soil fumigation. 2. Effects on bacteria. Soil Biol Biochem 8:249–253CrossRefGoogle Scholar
  39. Ruíz-Valdiviezo VM, Luna-Guido M, Galzy A, Gutiérrez-Miceli FA, Dendooven L (2010) Greenhouse gas emissions and C and N mineralization in soils of Chiapas (México) amended with leaves of piñón (Jatrophacurcas L.). Appl Soil Ecol 46:17–25CrossRefGoogle Scholar
  40. SAS Institute (1989) Statistic guide for personal computers, Version 6.04, Ed, SAS Institute, CaryGoogle Scholar
  41. Valenzuela-Encinas C, Neria-González I, Alcántara-Hernández RJ, Enríquez-Aragón JA, Estrada-Alvarado I, Hernández-Rodríguez C, Dendooven L, Marsch R (2008) Phylogenetic analysis of the archaeal community in an alkaline saline soil of the former lake Texcoco (Mexico). Extremophiles 12:247–254PubMedCrossRefGoogle Scholar
  42. Valenzuela-Encinas C, Neria-González I, Alcántara-Hernández RJ, Estrada-Alvarado I, Zavala-Díaz de la Serna FJ, Dendooven L, Marsch R (2009) Changes in the bacterial populations of the highly alkaline saline soil of the former lake Texcoco (Mexico) following flooding. Extremophiles 13:609–621PubMedCrossRefGoogle Scholar
  43. Vega-Járquin C, Valenzuela-Encinas C, Neri-González I, Alcántara-Hernández RJ, Hernández-Santiago MA, Luna-Guido ML, Marsch R, Dendooven L (2008) Is nitrate reduction to nitrite possible in glucose-amended alkaline saline soil under aerobic conditions? Soil Biol Biochem 40:2796–2802CrossRefGoogle Scholar
  44. 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 73:5261–5267PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2014

Authors and Affiliations

  • Juan M. Bello-López
    • 1
  • Cristina A. Domínguez-Mendoza
    • 1
  • Arit S. de León-Lorenzana
    • 1
  • Laura Delgado-Balbuena
    • 1
  • Yendi E. Navarro-Noya
    • 1
  • Selene Gómez-Acata
    • 1
  • Analine Rodríguez-Valentín
    • 1
  • Victor M. Ruíz-Valdiviezo
    • 1
  • Marco Luna-Guido
    • 1
  • Nele Verhulst
    • 2
  • Bram Govaerts
    • 2
  • Luc Dendooven
    • 1
  1. 1.Laboratory of Soil EcologyABACUS, Cinvestav, Avenida Instituto Politécnico Nacional 2508Mexico D.F.Mexico
  2. 2.International Maize and Wheat Improvement Centre (CIMMYT)Mexico D.F.Mexico

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