Abstract
The diversity of the dissimilatory and respiratory nitrate-reducing communities was studied in two soils of the former lake Texcoco (Mexico). Genes encoding the membrane-bound nitrate reductase (narG) and the periplasmic nitrate reductase (napA) were used as functional markers. To investigate bacterial communities containing napA and narG in saline alkaline soils of the former lake Texcoco, libraries of the two sites were constructed (soil T3 with pH 11 and electrolytic conductivity in saturated extract (ECSE) 160 dS m−1 and soil T1 with pH 8.5 and ECSE 0.8 dS m−1). Phylogenetic analysis of napA sequences separated the clone families into two main groups: dependent or independent of NapB. Most of napA sequences from site T1 were grouped in the NapB-dependent clade, meanwhile most of the napA sequences from the extreme soil T3 were affiliated to the NapB-independent group. For both sites, partial narG sequences were associated with representatives of the Proteobacteria, Firmicutes and Actinobacteria phyla, but the proportions of the clones were different. Our results support the concept of a specific and complex nitrate-reducing community for each soil of the former lake Texcoco.
Similar content being viewed by others
References
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402
Bedzyk L, Wang T, Ye RW (1999) The periplasmic nitrate reductase in Pseudomonas sp. strain G-179 catalyzes the first step of denitrification. J Bacteriol 181:2802–2806
Berks BC, Ferguson SJ, Moir JWB, Richardson DJ (1995a) Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochem Biophys Acta 1232:97–173
Berks BC, Richardson DJ, Reilly A, Willis AC, Ferguson SJ (1995b) The napEDABC gene cluster enconding the periplasmic nitrate reductase system of Thiosphaera pantotropa. Biochem J 309:983–992
Blasco F, Guigliarelli B, Magalon A, Asso M, Giordano G, Rothery RA (2001) The coordination and function of the redox centres of the membrane-bound nitrate reductases. Cell Mol Life Sci 58:179–193
Bru D, Sarr A, Philippot L (2007) Relative abundances of proteobacterial membrane-bound and periplasmic nitrate reductases in selected environments. Appl Environ Microbiol 73:5971–5974
Bursakov SA, Carneiro C, Almendra MJ, Duarte RO, Caldeira J, Moura I, Moura JJG (1997) Enzymatic properties and effect of ionic strength on periplasmic nitrate reductase (NAP) from Desulfovibrio desulfuricans ATCC 27774. Biochem Biophys Res Commun 239:816–822
Carter JP, Hsaio YH, Spiro S, Richardson DJ (1995) Soil and sediment bacteria capable of aerobic nitrate respiration. Appl Environ Microbiol 61:2852–2858
Castillo F, Dobao MM, Reyes F, Blasco R, Roldán MD, Gavira M, Caballero FJ, Martínez-Luque M (1996) Molecular and regulatory properties of the nitrate-reducing systems of Rhodobacter. Curr Microbiol 33:341–346
Castro-Silva C, Luna-Guido ML, Ceballos JM, Marsch R, Dendooven L (2008) Production of carbon dioxide and nitrous oxide in alkaline saline soil of texcoco at different water contents amended with urea: a laboratory study. Soil Biol Biochem 40:1813–1822
Chèneby D, Hallet S, Mondon M, Martin-Laurent F, Germon JC, Philippot L (2003) Genetic characterization of the nitrate-reducing community based on narG nucleotide sequence analysis. Microb Ecol 46:113–121
Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the clustal series of programs. Nucl Acids Res 31:3497–3500
Christensen S, Simkins S, Tiedje JM (1990) Temporal patterns of soil denitrification: their stability and causes. Soil Sci Soc Am J 54:1614–1618
Conde E, Cardenas M, Ponce-Mendoza A, Luna-Guido ML, Cruz-Mondragon 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
D’Haene K, Moreels E, Neve S, Chaves Daguilar B, Boeckx P, Hofman G, Cleemput O (2003) Soil properties influencing the denitrification potential of flemish agricultural soils. Biol Fert Soils 38:358–366
Dias JM, Than ME, Humm A, Huber R, Bourenkov GP, Bartunik HD, Bursakov S, Calvate J, Caldeira J, Carneiro C, Moura JJG, Moura I, Romao MJ (1999) Crystal structure of the first dissimilatory nitrate reductase at 1.9 Å solved by MAD methods. Structure 7:65–79
Eisle O, Kroneck PMH (2004) Structural basis of denitrification. Biol Chem 385:875–883
Flanagan DA, Gregory LG, Carter JP, Karakas-Sen A, Richardson DJ, Spiro S (1999) Detection of genes for periplasmic nitrate reductase in nitrate respiring bacteria and in community DNA. FEMS Microbiol Lett 177:263–270
Ghiglione J-F, Gourbiere F, Potier P, Philippot L, Lensi R (2000) Role of respiratory nitrate reductase in ability of Pseudomonas fluorescens YT101 to colonize the rhizosphere of maize. Appl Environ Microbiol 66:4012–4016
Giovannoni S, Rappé M (2000) Evolution, diversity, and molecular ecology of marine prokaryotes. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, New Jersey, pp 47–84
Gregory LG, Karakas-Sen A, Richardson DJ, Spiro S (2000) Detection of genes for membrane-bound nitrate reductase in nitrate-respiring bacteria and in community DNA. FEMS Microbiol Lett 183:275–279
Gregory LG, Bond PL, Richardson DJ, Spiro S (2003) Characterization of a nitrate-respiring bacterial community using the nitrate reductase gene (narG) as a functional marker. Microbiology 149:229–237
Jepson BJN, Marietou A, Mohan S, Cole JA, Butler CS, Richardson DJ (2006) Evolution of the soluble nitrate reductase: defining the monomeric periplasmic nitrate reductase subgroup. Biochem Soc Trans 34:122–126
Kisand V, Wikner J (2003) Limited resolution of 16S rDNA DGGE caused by melting properties and closely related DNA sequences. J Microbiol Methods 54:183–191
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
Luna-Guido ML, Beltrán-Hernández RI, Dendooven L (2001) Dynamics of 14C-labelled glucose in alkaline saline soil. Soil Biol Biochem 33:707–719
Moreno-Vivian C, Cabello P, Martinez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181:6573–6584
Mounier E, Hallet S, Cheneby D, Benizri E, Gruet Y, Nguyen C, Piutti S, Robin C, Slezack-Deschaumes S, Martin-Laurent F, Germon JC, Philippot L (2004) Influence of maize mucilage on the diversity and activity of the denitrifying community. Environ Microbiol 6:301–312
Nijburg JW, Laanbroek HJ (1997) The influence of Glyceria maxima and nitrate input on the composition and nitrate metabolism of the dissimilatory nitrate-reducing bacterial community. FEMS Microbiol Ecol 22:57–63
Nijburg JW, Coolen MJL, Gerards S, Gunnewiek P, Laanbroek HJ (1997) Effects of nitrate availability and the presence of Glyceria maxima on the composition and activity of the dissimilatory nitrate-reducing bacterial community. Appl Environ Microbiol 63:931–937
Nonaka H, Keresztes G, Shinoda Y, Ikenaga Y, Abe M, Naito K, Inatomi K, Furukawa K, Inui M, Yukawa H (2006) Complete genome sequence of the dehalorespiring bacterium Desulfitobacterium hafniense Y51 and comparison with Dehalococcoides ethenogenes 195. J Bacteriol 188:2262–2274
Page RDM (1996) Tree View: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
Philippot L (2002) Denitrifying genes in bacterial and archaeal genomes. BBA-Gene Struct Expr 1577:355–376
Philippot L, Clays-Josserand A, Lensi R (1995) Use of Tn5 mutants to assess the role of the dissimilatory nitrite reductase in the competitive abilities of two Pseudomonas strains in soil. Appl Environ Microbiol 61:1426–1430
Philippot L, Piutti S, Martin-Laurent F, Hallet S, Germon JC (2002) Molecular analysis of the nitrate-reducing community from unplanted and maize-planted soils. Appl Environ Microbiol 68:6121–6128
Philippot L, Kuffner M, Chèneby D, Depret G, Laguerre G, Martin-Laurent F (2006) Genetic structure and activity of the nitrate-reducers community in the rhizosphere of different cultivars of maize. Plant Soil 287:177–186
Potter LC, Millington P, Griffiths LH, Thomas GA, Cole J (1999) Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate-limited growth? Biochem J 344:77–84
Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ (2001) Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58:165–178
Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504
Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73:3612–3622
Sorokin D, Zhilina T, Lysenko A, Tourova T, Spiridonova E (2006) Metabolic versatility of haloalkaliphilic bacteria from soda lakes belonging to the Alkalispirillum–Alkalilimnicola group. Extremophiles 10:213–220
Stolz JF, Basu P (2002) Evolution of nitrate reductase: molecular and structural variations on a common function. ChemBioChem 3:198–206
Ueda K, Yamashita A, Ishikawa J, Shimada M, T-o Watsuji, Morimura K, Ikeda H, Hattori M, Beppu T (2004) Genome sequence of Symbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res 32:4937–4944
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
Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, Wu D, Paulsen I, Nelson KE, Nelson W, Fouts DE, Levy S, Knap AH, Lomas MW, Nealson K, White O, Peterson J, Hoffman J, Parsons R, Baden-Tillson H, Pfannkoch C, Rogers Y-H, Smith HO (2004) Environmental genome shotgun sequencing of the sargasso sea. Science 304:66–74
Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699
Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616
Acknowledgments
The research was funded by “Secretaria de Medio Ambiente y Recursos Naturales” (SEMARNAT) project SEMARNAT-2004-C01-257 and “Consejo Nacional de Ciencia y Tecnología” (CONACYT) project SEP-1004-C01-479991.I·N. We thank Soledad Vásquez-Murrieta and Erick Ruiz-Romero for providing soil samples from Xochimilco and Texcoco and Francisco Javier Zavala de la Serna for revising the manuscript. R.A.-H. and C.V.-E. received grant-aided support from CONACYT.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. Matsunaga.
Rights and permissions
About this article
Cite this article
Alcántara-Hernández, R.J., Valenzuela-Encinas, C., Marsch, R. et al. Respiratory and dissimilatory nitrate-reducing communities from an extreme saline alkaline soil of the former lake Texcoco (Mexico). Extremophiles 13, 169–178 (2009). https://doi.org/10.1007/s00792-008-0207-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-008-0207-1