Skip to main content
SpringerLink
Log in

Changes in methane oxidation activity and methanotrophic community composition in saline alkaline soils

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

Abstract

The soil of the former Lake Texcoco is a saline alkaline environment where anthropogenic drainage in some areas has reduced salt content and pH. Potential methane (CH4) consumption rates were measured in three soils of the former Lake Texcoco with different electrolytic conductivity (EC) and pH, i.e. Tex-S1 a >18 years drained soil (EC 0.7 dS m−1, pH 8.5), Tex-S2 drained for ~10 years (EC 9.0 dS m−1, pH 10.3) and the undrained Tex-S3 (EC 84.8 dS m−1, pH 10.3). An arable soil from Alcholoya (EC 0.7 dS m−1, pH 6.7), located nearby Lake Texcoco was used as control. Methane oxidation in the soil Tex-S1 (lowest EC and pH) was similar to that in the arable soil from Alcholoya (32.5 and 34.7 mg CH4 kg−1 dry soil day−1, respectively). Meanwhile, in soils Tex-S2 and Tex-S3, the potential CH4 oxidation rates were only 15.0 and 12.8 mg CH4 kg−1 dry soil day−1, respectively. Differences in CH4 oxidation were also related to changes in the methane-oxidizing communities in these soils. Sequence analysis of pmoA gene showed that soils differed in the identity and number of methanotrophic phylotypes. The Alcholoya soil and Tex-S1 contained phylotypes grouped within the upland soil cluster gamma and the Jasper Ridge, California JR-2 clade. In soil Tex-S3, a phylotype related to Methylomicrobium alcaliphilum was detected.

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

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res 25:3389–3402

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Antony CP, Kumaresan D, Ferrando L, Boden R, Moussard H, Scavino AF, Shouche YS, Murrell JC (2010) Active methylotrophs in the sediments of Lonar Lake, a saline and alkaline ecosystem formed by meteor impact. ISME J 4:1470–1480

    Article  PubMed  CAS  Google Scholar 

  • Antony CP, Kumaresan D, Hunger S, Drake HL, Murrell JC, Shouche YS (2012) Microbiology of Lonar Lake and other soda lakes. ISME J 7:468–476

    Article  PubMed  CAS  Google Scholar 

  • Avnimelech Y, Ritvo G, Meijer LE, Kochba M (2001) Water content, organic carbon and dry bulk density in flooded sediments. Aquac Eng 25:25–33

    Article  Google Scholar 

  • Bárcena TG, Finster KW, Yde JC (2011) Spatial patterns of soil development, methane oxidation, and methanotrophic diversity along a receding glacier forefield, Southeast Greenland. Arct Antarct Alp Res 43:178–188

    Article  Google Scholar 

  • Bedard C, Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH4 +, and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev 53:68–84

    PubMed Central  PubMed  CAS  Google Scholar 

  • Betancur-Galvis LA, Carrillo H, Luna-Guido M, Marsch R, Dendooven L (2012) Enhanced dissipation of polycyclic aromatic hydrocarbons in the rhizosphere of the Athel Tamarisk (Tamarix aphylla L. Karst.) grown in saline-alkaline soils of the former lake Texcoco. Int J Phytoremediation 14:741–753

    Article  PubMed  CAS  Google Scholar 

  • Bissett A, Abell GCJ, Bodrossy L, Richardson AE, Thrall PH (2012) Methanotrophic communities in Australian woodland soils of varying salinity. FEMS Microbiol Ecol 80:685–695

    Article  PubMed  CAS  Google Scholar 

  • Bodrossy L, Holmes EM, Holmes AJ, Kovács KL, Murrell JC (1997) Analysis of 16S rRNA and methane monooxygenase gene sequences reveals a novel group of thermotolerant and thermophilic methanotrophs, Methylocaldum gen. nov. Arch Microbiol 168:493–503

    Article  PubMed  CAS  Google Scholar 

  • Bourne DG, McDonald IR, Murrell JC (2001) Comparison of pmoA PCR primer sets as tools for investigating methanotroph diversity in three Danish soils. Appl Environ Microbiol 67:3802–3809

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bowman J (2006) The methanotrophs-the families Methylococcaceae and Methylocystaceae Ch. 3.1.14. Prokaryotes 5:266–289

    Article  Google Scholar 

  • Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinform 4:29

    Article  Google Scholar 

  • Ceja-Navarro JA, Rivera FN, Patiño-Zúñiga L, Govaerts B, Marsch R, Vila-Sanjurjo A, Dendooven L (2010) Molecular characterization of soil bacterial communities in contrasting zero tillage systems. Plant Soil 329:127–137

    Article  CAS  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Conde E, Cardenas M, Ponce-Mendoza A, Luna-Guido ML, Cruz-Mondragón C, Dendooven L (2005) The impacts of inorganic nitrogen application on mineralization of 14C-labelled maize and glucose, and on priming effect in saline alkaline soil. Soil Biol Biochem 37:681–691

    Article  CAS  Google Scholar 

  • Conrad R, Frenzel P, Cohen Y (1995) Methane emission from hypersaline microbial mats: lack of aerobic methane oxidation activity. FEMS Microbiol Ecol 16:297–305

    Article  CAS  Google Scholar 

  • Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074

    PubMed Central  PubMed  CAS  Google Scholar 

  • Cullen DW, Hirsch PR (1998) Simple and rapid method for direct extraction of microbial DNA from soil for PCR. Soil Biol Biochem 30:983–993

    Article  CAS  Google Scholar 

  • Dalal R, Allen D, Livesley S, Richards G (2008) Magnitude and biophysical regulators of methane emission and consumption in the Australian agricultural, forest, and submerged landscapes: a review. Plant Soil 309:43–76

    Article  CAS  Google Scholar 

  • Dedysh SN, Knief C, Dunfield PF (2005) Methylocella species are facultatively methanotrophic. J Bacteriol 187:4665–4670

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Degelmann DM, Borken W, Drake HL, Kolb S (2010) Different atmospheric methane-oxidizing communities in European beech and Norway spruce soils. Appl Environ Microbiol 76:3228–3235

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dendooven L, Alcántara-Hernández RJ, Valenzuela-Encinas C, Luna-Guido ML, 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 

  • Dörr N, Glaser B, Kolb S (2010) Methanotrophic communities in Brazilian ferralsols from naturally forested, afforested, and agricultural sites. Appl Environ Microbiol 76:1307–1310

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dumont MG, Murrell JC (2005) Community-level analysis: key genes of aerobic methane oxidation. Methods Enzymol 397:413–427

    Article  PubMed  CAS  Google Scholar 

  • Eshinimaev BT, Khmelenina VN, Trotsenko YA (2008) First isolation of a type II methanotroph from a soda lake. Microbiology 77:628–631

    Article  CAS  Google Scholar 

  • Fernández-Buces N, Siebe C, Cram S, Palacio JL (2006) Mapping soil salinity using a combined spectral response index for bare soil and vegetation: a case study in the former lake Texcoco, Mexico. J Arid Environ 65:644–667

    Article  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Guo C, Sun W, Harsh JB, Ogram A (1997) Hybridization analysis of microbial DNA from fuel oil-contaminated and non contaminated soil. Microb Ecol 34:178–187

    Article  PubMed  CAS  Google Scholar 

  • Gutiérrez-Castorena MDC, Stoops G, Ortiz-Solorio CA, López-Avila G (2005) Amorphous silica materials in soils and sediments of the Ex-Lago de Texcoco, Mexico: an explanation for its subsidence. Catena 60:205–226

    Article  CAS  Google Scholar 

  • Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241

    Article  PubMed  CAS  Google Scholar 

  • Han B, Chen Y, Abell G, Jiang H, Bodrossy L, Zhao J, Murrell JC, Xing XH (2009) Diversity and activity of methanotrophs in alkaline soil from a Chinese coal mine. FEMS Microbiol Ecol 70:196–207

    Article  CAS  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    PubMed Central  PubMed  CAS  Google Scholar 

  • Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132:203–208

    Article  PubMed  CAS  Google Scholar 

  • Holmes AJ, Roslev P, McDonald IR, Iversen N, Henriksen K, Murrell JC (1999) Characterization of methanotrophic bacterial populations in soils showing atmospheric methane uptake. Appl Environ Microbiol 65:3312–3318

    PubMed Central  PubMed  CAS  Google Scholar 

  • Horz HP, Rich V, Avrahami S, Bohannan BJM (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl Environ Microbiol 71:2642–2652

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jensen S, Neufeld JD, Birkeland NK, Hovland M, Murrell JC (2008) Methane assimilation and trophic interactions with marine Methylomicrobium in deep-water coral reef sediment off the coast of Norway. FEMS Microbiol Ecol 66:320–330

    Article  PubMed  CAS  Google Scholar 

  • Jones RD, Morita RY (1983) Methane oxidation by Nitrosococcus oceanus and Nitrosomonas europaea. Appl Environ Microbiol 45:401–410

    PubMed Central  PubMed  CAS  Google Scholar 

  • Jones BE, Grant WD, Duckworth AW, Owenson GG (1998) Microbial diversity of soda lakes. Extremophiles 2:191–200

    Article  PubMed  CAS  Google Scholar 

  • Khmelenina VN, Kalyuzhnaya MG, Starostina NG, Suzina NE, Trotsenko YA (1997) Isolation and characterization of halotolerant alkaliphilic methanotrophic bacteria from Tuva soda Lakes. Curr Microbiol 35:257–261

    Article  CAS  Google Scholar 

  • Khmelenina VN, Eshinimaev BT, Kalyuzhnaya MG, Trotsenko I (2000) Potential activity of methane and ammonia oxidation by methanotrophic communities from soda lakes of the southern Transbaikal. Mikrobiologiia 69:553–558

    PubMed  CAS  Google Scholar 

  • Knief C, Lipski A, Dunfield PF (2003) Diversity and activity of methanotrophic bacteria in different upland soils. Appl Environ Microbiol 69:6703–6714

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Levine UY, Teal TK, Robertson GP, Schmidt TM (2011) Agriculture’s impact on microbial diversity and associated fluxes of carbon dioxide and methane. ISME J 5:1683–1691

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lin JL, Radajewski S, Eshinimaev BT, Trotsenko YA, McDonald IR, Murrell JC (2004) Molecular diversity of methanotrophs in Transbaikal soda lake sediments and identification of potentially active populations by stable isotope probing. Environ Microbiol 6:1049–1060

    Article  PubMed  CAS  Google Scholar 

  • Lin JL, Joye SB, Scholten JC, Schafer H, McDonald IR, Murrell JC (2005) Analysis of methane monooxygenase genes in mono lake suggests that increased methane oxidation activity may correlate with a change in methanotroph community structure. Appl Environ Microbiol 71:6458–6462

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lüke C, Frenzel P (2011) Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77:6305–6309

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lüke C, Krause S, Cavigiolo S, Greppi D, Lupotto E, Frenzel P (2010) Biogeography of wetland rice methanotrophs. Environ Microbiol 12:862–872

    Article  PubMed  CAS  Google Scholar 

  • Luna-Guido ML, Beltrán-Hernández RI, Solís-Ceballos NA, Hernández-Chávez N, Mercado-García F, Catt JA, Olalde-Portugal V, Dendooven L (2000) Chemical and biological characteristics of alkaline saline soils from the former Lake Texcoco as affected by artificial drainage. Biol Fertil Soils 32:102–108

    Article  CAS  Google Scholar 

  • McDonald IR, Bodrossy L, Chen Y, Murrell JC (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74:1305–1315

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Murrell JC, Gilbert B, McDonald IR (2000) Molecular biology and regulation of methane monooxygenase. Arch Microbiol 173:325–332

    Article  PubMed  CAS  Google Scholar 

  • Nakamura T, Hoaki T, Hanada S, Maruyama A, Kamagata Y, Fuse H (2007) Soluble and particulate methane monooxygenase gene clusters in the marine methanotroph Methylomicrobium sp. strain NI. FEMS Microbiol Lett 277:157–164

    Article  PubMed  CAS  Google Scholar 

  • Op den Camp H, Islam T, Stott M, Harhangi H, Hynes A, Schouten S, Jetten M, Birkeland N-K, Pol A, Dunfield P (2009) Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 1:293–306

    Article  PubMed  CAS  Google Scholar 

  • Pester M, Friedrich MW, Schink B, Brune A (2004) pmoA-based analysis of methanotrophs in a littoral lake sediment reveals a diverse and stable community in a dynamic environment. Appl Environ Microbiol 70:3138–3142

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rambaut A (2007) FigTree, a graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/

  • 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 

  • Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531

    PubMed  CAS  Google Scholar 

  • Serrano-Silva N, Luna-Guido M, Fernández-Luqueño F, Marsch R, Dendooven L (2011) Emission of greenhouse gases from an agricultural soil amended with urea: a laboratory study. Appl Soil Ecol 47:92–97

    Article  Google Scholar 

  • Singh BK, Tate KR, Ross DJ, Singh J, Dando J, Thomas N, Millard P, Murrell JC (2009) Soil methane oxidation and methanotroph responses to afforestation of pastures with Pinus radiata stands. Soil Biol Biochem 41:2196–2205

    Article  CAS  Google Scholar 

  • Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A (2003) Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 54:779–791

    Article  Google Scholar 

  • Sorokin DY, Kuenen JG (2005) Chemolithotrophic haloalkaliphiles from soda lakes. FEMS Microbiol Ecol 52:287–295

    Article  PubMed  CAS  Google Scholar 

  • Sorokin DY, Jones BE, Kuenen JG (2000) A novel obligately methylotrophic, methane-oxidizing Methylomicrobium species from a highly alkaline environment. Extremophiles 4:145–155

    Article  PubMed  CAS  Google Scholar 

  • Stoecker K, Bendinger B, Schöning B, Nielsen PH, Nielsen JL, Baranyi C, Toenshoff ER, Daims H, Wagner M (2006) Cohn’s Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase. Proc Natl Acad Sci USA 103:2363–2367

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Trotsenko YA, Khmelenina VN (2002) Biology of extremophilic and extremotolerant methanotrophs. Arch Microbiol 177:123–131

    Article  PubMed  CAS  Google Scholar 

  • Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63:183–229

    Article  PubMed  CAS  Google Scholar 

  • Trotsenko YA, Medvedkova KA, Khmelenina VN, Eshinimayev BT (2009) Thermophilic and thermotolerant aerobic methanotrophs. Microbiology 78:387–401

    Article  CAS  Google Scholar 

  • Valenzuela-Encinas C, Neria-González I, Alcántara-Hernández R, Enríquez-Aragón J, 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  PubMed  CAS  Google Scholar 

  • Valenzuela-Encinas C, Neria-Gonzalez I, Alcantara-Hernandez RJ, Estrada-Alvarado I, de la Serna FJZD, 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 

  • Valenzuela-Encinas C, Alcántara-Hernández RJ, Estrada-Alvarado I, de la Serna FJZD, Dendooven L, Marsch R (2012) The archaeal diversity and population in a drained alkaline saline soil of the former lake Texcoco (Mexico). Geomicrobiology 29:18–22

    Article  Google Scholar 

  • Völker H, Schweisfurth R, Hirsch P (1977) Morphology and ultrastructure of Crenothrix polyspora Cohn. J Bacteriol 131:306–313

    PubMed Central  PubMed  Google Scholar 

  • Vorobev AV, Baani M, Doronina NV, Brady AL, Liesack W, Dunfield PF, Dedysh SN (2011) Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase. Int J Syst Evol Microbiol 61:2456–2463

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Li Z, Ning T, Gu S (2011) Methane uptake in salt-affected soils shows low sensitivity to salt addition. Soil Biol Biochem 43:1434–1439

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research was funded by “Consejo Nacional de Ciencia y Tecnología” (CONACYT) project CB‐2010‐01-153216. N. S.-S., R. J. A.-H. and C. V.-E. received grant-aided support from CONACYT.

Author information

Authors and Affiliations

  1. Laboratory of Soil Ecology, ABACUS, Cinvestav, Campus Zacatenco, 07360, Mexico D.F., Mexico

    Nancy Serrano-Silva, Rodolfo Marsch & Luc Dendooven

  2. Department of Chemistry, Unidad Profesional Interdisciplinaria de Biotecnologia-IPN (UPIBI), 07340, Mexico D.F., Mexico

    César Valenzuela-Encinas

  3. Laboratorio de Ecología Molecular y Epigenética, Instituto de Ecología, Universidad Nacional Autónoma de México, Circuito Exterior sn. Ciudad Universitaria, Del. Coyoacán, 04510, Mexico D.F., Mexico

    Rocio J. Alcántara-Hernández

Authors
  1. Nancy Serrano-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. César Valenzuela-Encinas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodolfo Marsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luc Dendooven
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rocio J. Alcántara-Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rocio J. Alcántara-Hernández.

Additional information

Communicated by A. Oren.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Serrano-Silva, N., Valenzuela-Encinas, C., Marsch, R. et al. Changes in methane oxidation activity and methanotrophic community composition in saline alkaline soils. Extremophiles 18, 561–571 (2014). https://doi.org/10.1007/s00792-014-0641-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-014-0641-1

Keywords

Search

Navigation