Skip to main content
SpringerLink
Log in

Bacterial colonization of a fumigated alkaline saline soil

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 430:551–553

    Article  CAS  PubMed  Google Scholar 

  • 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 35:390–403

    Article  Google Scholar 

  • Cano RJ, Borucki MK (1995) Revival and identification of bacterial spores in 25- to 40-million-year-old dominican amber. Science 268:1060–1064

    Article  CAS  PubMed  Google Scholar 

  • 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 26:266–267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 7:335–336

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 76:3685–3691

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 51:741–746

    Article  PubMed  Google Scholar 

  • 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 40:4317–4325

    Article  CAS  PubMed  Google Scholar 

  • de la Haba RR, Sánchez-Porro C, Marquez MC, Ventosa A (2011) Taxonomy of halophiles. In: Horikoshi K (ed) Extremophiles handbook, Springer, Berlin, pp 256–308

  • 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 42:865–877

    Article  CAS  Google Scholar 

  • 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 73:122–129

    Article  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • 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 54:187–193

    Article  Google Scholar 

  • Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • 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 58:1855–1859

    Article  Google Scholar 

  • 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 21:494–504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 4:17–27

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 164:189–198

    Article  CAS  PubMed  Google Scholar 

  • Horikoshi K (1999) Alkaliphiles: some applications of their products for biotechnology. Microbiol Mol Biol R 63:735–750

    CAS  Google Scholar 

  • Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil. V. A method for measuring soil biomass. Soil Biol Biochem 8:209–213

    Article  CAS  Google Scholar 

  • 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 3:442–453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 40:61–73

    Article  CAS  Google Scholar 

  • Keshri J, Mishra A, Jha B (2013) Microbial population index and community structure in saline–alkaline soil using gene targeted metagenomics. Microbiol Res 168:165–173

    Article  CAS  PubMed  Google Scholar 

  • Kolter R, Siegele DA, Tormo A (1993) The stationary phase of the bacterial life cycle. Ann Rev Microbiol 47:855–874

    Article  CAS  Google Scholar 

  • 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 66:40–48

    Article  CAS  PubMed  Google Scholar 

  • 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 32:102–108

    Article  CAS  Google Scholar 

  • 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 250:29–38

    Article  CAS  Google Scholar 

  • 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 8:6

    Article  Google Scholar 

  • 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 24:179–181

    Article  Google Scholar 

  • 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 78:7398–7406

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 65:86–95

    Article  CAS  Google Scholar 

  • 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 31:152–160

    Article  CAS  Google Scholar 

  • Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol R 63:334–348

    CAS  Google Scholar 

  • Partanen P, Hultman J, Paulin L, Auvinen P, Romantschuk M (2010) Bacterial diversity at different stages of the composting process. BMC Microbiol 10:94

    Article  PubMed Central  PubMed  Google Scholar 

  • Pathma J, Sakthivel N (2013) Molecular and functional characterization of bacteria isolated from straw and goat manure based vermicompost. Appl Soil Ecol 70:33–47

    Article  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 36:269–275

    Article  Google Scholar 

  • Ridge EH (1976) Studies on soil fumigation. 2. Effects on bacteria. Soil Biol Biochem 8:249–253

    Article  CAS  Google Scholar 

  • 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 46:17–25

    Article  Google Scholar 

  • SAS Institute (1989) Statistic guide for personal computers, Version 6.04, Ed, SAS Institute, Cary

  • 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 12:247–254

    Article  CAS  PubMed  Google Scholar 

  • 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 13:609–621

    Article  PubMed  Google Scholar 

  • 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 40:2796–2802

    Article  Google Scholar 

  • 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  CAS  PubMed Central  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Laboratory of Soil Ecology, ABACUS, Cinvestav, Avenida Instituto Politécnico Nacional 2508, 07360, Mexico D.F., Mexico

    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 & Luc Dendooven

  2. International Maize and Wheat Improvement Centre (CIMMYT), Mexico D.F., Mexico

    Nele Verhulst & Bram Govaerts

Authors
  1. Juan M. Bello-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristina A. Domínguez-Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arit S. de León-Lorenzana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura Delgado-Balbuena
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yendi E. Navarro-Noya
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Selene Gómez-Acata
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Analine Rodríguez-Valentín
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Victor M. Ruíz-Valdiviezo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marco Luna-Guido
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nele Verhulst
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Bram Govaerts
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Luc Dendooven
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luc Dendooven.

Additional information

Communicated by A. Oren.

Electronic supplementary material

Below is the link to the electronic supplementary material.

792_2014_653_MOESM1_ESM.pdf

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

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)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bello-López, J.M., Domínguez-Mendoza, C.A., de León-Lorenzana, A.S. et al. Bacterial colonization of a fumigated alkaline saline soil. Extremophiles 18, 733–743 (2014). https://doi.org/10.1007/s00792-014-0653-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-014-0653-x

Keywords

Search

Navigation