La versión final de este artículo es de uso interno de la institución.
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


The description of the diversity and structure of microbial communities through quantification of the constituent populations is one of the major objectives in environmental microbiology. The implications of models for community assembly are practical as well as theoretical, because the extent of biodiversity is thought to influence the function of ecosystems. Current attempts to predict species diversity in different environments derive the numbers of individuals for each operational taxonomic unit (OTU) from the frequency of clones in 16S rDNA gene libraries, which are subjected to a number of inherent biases and artefacts. We show that diversity of the bacterial community present in a complex microbial ensemble can be estimated by fitting the data of the full-cycle rRNA approach to a model of species abundance distribution. Sequences from a 16S rDNA gene library from activated sludge were reliably assigned to OTUs at a genetic distance of 0.04. A group of 17 newly designed rRNA-targeted oligonucleotide probes were used to quantify by fluorescence in situ hybridization, OTUs represented with more than three clones in the 16S rDNA clone library. Cell abundance distribution was best described by a geometric series, after the goodness of fit was evaluated by the Kolmogorov-Smirnov test. Although a complete mechanistic understanding of all the ecological processes involved is still not feasible, describing the distribution pattern of a complex bacterial assemblage model can shed light on the way bacterial communities operate. © 2007 The Authors.


Documento: Artículo
Título:Bacterial taxa abundance pattern in an industrial wastewater treatment system determined by the full rRNA cycle approach
Autor:Figuerola, E.L.M.; Erijman, L.
Filiación:Instituto de Investigaciones en Ingenieria Genetica Y Biologia Molecular (INGEBI-CONICET), Facultad de Ciencias Exactas Y Naturales, Universidad de Buenos Aires, Vuelta de Obligado 2490, (ADN1428) Buenos Aires, Argentina
Palabras clave:primer DNA; RNA 16S; article; bacterium; biodiversity; biological model; DNA sequence; fluorescence in situ hybridization; fluorescence microscopy; gene library; genetics; microbiology; molecular genetics; nonparametric test; nucleotide sequence; phylogeny; sewage; water management; Bacteria; Base Sequence; Biodiversity; DNA Primers; Environmental Microbiology; Gene Library; In Situ Hybridization, Fluorescence; Microscopy, Fluorescence; Models, Biological; Molecular Sequence Data; Phylogeny; RNA, Ribosomal, 16S; Sequence Analysis, DNA; Sewage; Statistics, Nonparametric; Waste Disposal, Fluid; Water Microbiology; Water Purification; Bacteria (microorganisms); Otus
Página de inicio:1780
Página de fin:1789
Título revista:Environmental Microbiology
Título revista abreviado:Environ. Microbiol.
CAS:DNA Primers; RNA, Ribosomal, 16S; Sewage


  • Acinas, S.G., Sarma-Rupavtarm, R., Klepac-Ceraj, V., Polz, M.F., PCR-induced sequence artifacts and bias: Insights from comparison of two 16S rRNA clone libraries constructed from the same sample (2005) Appl Environ Microbiol, 71, pp. 8966-8969
  • Alm, E.W., Oerther, D.B., Larsen, N., Stahl, D.A., Raskin, L., The oligonucleotide probe database (1996) Appl Environ Microbiol, 62, pp. 3557-3559
  • Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool (1990) J Mol Biol, 215, pp. 403-410
  • Amann, R.I., Ludwig, W., Schleifer, K.H., Phylogenetic identification and in situ detection of individual microbial cells without cultivation (1995) Microbiol Rev, 59, pp. 143-169
  • Bell, T., Newman, J.A., Silverman, B.W., Turner, S.L., Lilley, A.K., The contribution of species richness and composition to bacterial services (2005) Nature, 436, pp. 1157-1160
  • Bramucci, M., Kane, H., Chen, M., Nagarajan, V., Bacterial diversity in an industrial wastewater bioreactor (2003) Appl Microbiol Biotechnol, 62, pp. 594-600
  • Briones, A., Raskin, L., Diversity and dynamics of microbial communities in engineered environments and their implications for process stability (2003) Curr Opin Biotechnol, 14, pp. 270-276
  • Casamayor, E.O., Pedros-Alio, C., Muyzer, G., Amann, R., Microheterogeneity in 16S ribosomal DNA-defined bacterial populations from a stratified planktonic environment is related to temporal changes and to ecological adaptations (2002) Appl Environ Microbiol, 68, pp. 1706-1714
  • Cole, J.R., Chai, B., Farris, R.J., Wang, Q., Kulam, S.A., McGarrell, D.M., The Ribosomal Database Project (RDP-II): Sequences and tools for high-throughput rRNA analysis (2005) Nucleic Acids Res, 33, pp. D294-D296
  • Coleman, M.L., Sullivan, M.B., Martiny, A.C., Steglich, C., Barry, K., Delong, E.F., Chisholm, S.W., Genomic islands and the ecology and evolution of Prochlorococcus (2006) Science, 311, pp. 1768-1770
  • Coskuner, G., Ballinger, S.J., Davenport, R.J., Pickering, R.L., Solera, R., Head, I.M., Curtis, T.P., Agreement between theory and measurement in quantification of ammonia-oxidizing bacteria (2005) Appl Environ Microbiol, 71, pp. 6325-6334
  • Curtis, T.P., Sloan, W.T., Prokaryotic diversity and its limits: Microbial community structure in nature and implications for microbial ecology (2004) Curr Opin Microbiol, 7, pp. 221-226
  • Curtis, T.P., Sloan, W.T., Scannell, J.W., Estimating prokaryotic diversity and its limits (2002) Proc Natl Acad Sci USA, 99, pp. 10494-10499
  • Daims, H., Ramsing, N.B., Schleifer, K.H., Wagner, M., Cultivation-independent, semiautomatic determination of absolute bacterial cell numbers in environmental samples by fluorescence in situ hybridization (2001) Appl Environ Microbiol, 67, pp. 5810-5818
  • Daims, H., Lucker, S., Wagner, M., DAIME, a novel image analysis program for microbial ecology and biofilm research (2006) Environ Microbiol, 8, pp. 200-213
  • Davenport, R.J., Curtis, T.P., Quantitative fluorescence in situ hibridisation (FISH): Statistical methods for valid cell counting (2004) Molecular Microbial Ecology Manual., pp. 1487-1516. , In. Kowalchuk, G.A., de Bruijn, F.J., Head, I.M., Akkermans, A.D.L. van Elsas, J.D. (eds). Dordrecht, the Netherlands: Kluwer Academic, pp
  • Davenport, R.J., Curtis, T.P., Goodfellow, M., Stainsby, F.M., Bingley, M., Quantitative use of fluorescent in situ hybridization to examine relationships between mycolic acid-containing actinomycetes and foaming in activated sludge plants (2000) Appl Environ Microbiol, 66, pp. 1158-1166
  • Eschenhagen, M., Schuppler, M., Roske, I., Molecular characterization of the microbial community structure in two activated sludge systems for the advanced treatment of domestic effluents (2003) Water Res, 37, pp. 3224-3232
  • Fernandez, A., Huang, S.Y., Seston, S., Xing, J., Hickey, R., Criddle, C., Tiedje, J., How stable is stable? Function versus community composition (1999) Appl Environ Microbiol, 65, pp. 3697-3704
  • Good, I.J., The population frequencies of species and the estimation of population parameters (1953) Biometrika, 40, pp. 237-264
  • Hahn, M.W., Pockl, M., Ecotypes of planktonic actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats (2005) Appl Environ Microbiol, 71, pp. 766-773
  • Hong, S.H., Bunge, J., Jeon, S.O., Epstein, S.S., Predicting microbial species richness (2006) Proc Natl Acad Sci USA, 103, pp. 117-122
  • Horner-Devine, M.C., Carney, K.M., Bohannan, B.J., An ecological perspective on bacterial biodiversity (2004) Proc Biol Sci, 271, pp. 113-122
  • Hubbell, S.P., (2001) The Unified Neutral Theory of Biodiversity and Biogeography., , Princeton, NJ, USA: Princeton University Press
  • Hugenholtz, P., Huber, T., Chimeric 16S rDNA sequences of diverse origin are accumulating in the public databases (2003) Int J Syst Evol Microbiol, 53, pp. 289-293
  • Jaspers, E., Overmann, J., Ecological significance of microdiversity: Identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies (2004) Appl Environ Microbiol, 70, pp. 4831-4839
  • Juretschko, S., Loy, A., Lehner, A., Wagner, M., The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach (2002) Syst Appl Microbiol, 25, pp. 84-99
  • Kowalchuk, G.A., Stephen, J.R., De Boer, W., Prosser, J.I., Embley, T.M., Woldendorp, J.W., Analysis of ammonia-oxidizing bacteria of the beta subdivision of the class Proteobacteria in coastal sand dunes by denaturing gradient gel electrophoresis and sequencing of PCR-amplified 16S ribosomal DNA fragments (1997) Appl Environ Microbiol, 63, pp. 1489-1497
  • Kurata, S., Kanagawa, T., Magariyama, Y., Takatsu, K., Yamada, K., Yokomaku, T., Kamagata, Y., Reevaluation and reduction of a PCR bias caused by reannealing of templates (2004) Appl Environ Microbiol, 70, pp. 7545-7549
  • Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A., Biodiversity and ecosystem functioning: Current knowledge and future challenges (2001) Science, 294, pp. 804-808
  • Lozada, M., Itria, R.F., Figuerola, E.L.M., Babay, P.A., Gettar, R.T., De Tullio, L.A., Erijman, L., Bacterial community shifts in nonylphenol polyethoxylates-enriched activated sludge (2004) Water Res, 38, pp. 2077-2086
  • Lozada, M., Figuerola, E.L., Itria, R.F., Erijman, L., Replicability of dominant bacterial populations after long-term surfactant-enrichment in lab-scale activated sludge (2006) Environ Microbiol, 8, pp. 625-638
  • Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, ARB: A software environment for sequence data (2004) Nucleic Acids Res, 32, pp. 1363-1371
  • Lunn, M., Sloan, W.T., Curtis, T.P., Estimating bacterial diversity from clone libraries with flat rank abundance distributions (2004) Environ Microbiol, 6, pp. 1081-1085
  • Luyten, Y.A., Thompson, J.R., Morrill, W., Polz, M.F., Distel, D.L., Extensive variation in intracellular symbiont community composition among members of a single population of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae) (2006) Appl Environ Microbiol, 72, pp. 412-417
  • Magurran, A.E., (2004) Measuring Biological Diversity., , Oxford, UK: Blackwell Publishing
  • Magurran, A.E., Ecology: Linking species diversity and genetic diversity (2005) Curr Biol, 15, pp. R597-R599
  • Magurran, A.E., Biological diversity (2005) Curr Biol, 15, pp. R116-R118
  • Magurran, A.E., Henderson, P.A., Explaining the excess of rare species in natural species abundance distributions (2003) Nature, 422, pp. 714-716
  • Manz, W., Wagner, M., Amann, R., Schleifer, K.-H., In situ characterization of the microbial consortia active in two wastewater treatment plants (1994) Water Res, 28, pp. 1715-1723
  • May, R.M., Patterns of species abundance and diversity (1975) Ecology and Evolution of Communities., pp. 81-120. , In. Cody, M.L. Diamond, J.M. (eds). Cambridge, MA, USA: Harvard University Press, pp
  • Mota, C., Head, M.A., Ridenoure, J.A., Cheng, J.J., De Los Reyes, F.L., Effects of aeration cycles on nitrifying bacterial populations and nitrogen removal in intermittently aerated reactors (2005) Appl Environ Microbiol, 71, pp. 8565-8572. , III (
  • O'Mullan, G.D., Ward, B.B., Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterey Bay, California (2005) Appl Environ Microbiol, 71, pp. 697-705
  • Pernthaler, A., Pernthaler, J., Amann, R., Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria (2002) Appl Environ Microbiol, 68, pp. 3094-3101
  • Pernthaler, J., Pernthaler, A., Amann, R., Automated enumeration of groups of marine picoplankton after fluorescence in situ hybridization (2003) Appl Environ Microbiol, 69, pp. 2631-2637
  • Pielou, E.C., (1975) Ecological Diversity., , New York, NY, USA: Wiley Interscience
  • Polz, M.F., Cavanaugh, C.M., Bias in template-to-product ratios in multitemplate PCR (1998) Appl Environ Microbiol, 64, pp. 3724-3730
  • Qiu, X.Y., Wu, L.Y., Huang, H.S., McDonel, P.E., Palumbo, A.V., Tiedje, J.M., Zhou, J.Z., Evaluation of PCR-generated chimeras: Mutations, and heteroduplexes with 16S rRNA gene-based cloning (2001) Appl Environ Microbiol, 67, pp. 880-887
  • Rittmann, B.E., Laspidou, C.S., Flax, J., Stahl, D.A., Urbain, V., Harduin, H., Molecular and modeling analyses of the structure and function of nitrifying activated sludge (1999) Water Sci Technol, 39, pp. 51-59
  • Schloss, P.D., Handelsman, J., Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness (2005) Appl Environ Microbiol, 71, pp. 1501-1506
  • Schramm, A., Fuchs, B.M., Nielsen, J.L., Tonolla, M., Stahl, D.A., Fluorescence in situ hybridization of 16S rRNA gene clones (Clone-FISH) for probe validation and screening of clone libraries (2002) Environ Microbiol, 4, pp. 713-720
  • Sekar, R., Pernthaler, A., Pernthaler, J., Warnecke, F., Posch, T., Amann, R., An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization (2003) Appl Environ Microbiol, 69, pp. 2928-2935
  • Sloan, W.T., Lunn, M., Woodcock, S., Head, I.M., Nee, S., Curtis, T.P., Quantifying the roles of immigration and chance in shaping prokaryote community structure (2006) Environ Microbiol, 8, pp. 732-740
  • Snaidr, J., Amann, R., Huber, I., Ludwig, W., Schleifer, K.-H., Phylogenetic analysis and in situ identification of bacteria in activated sludge (1997) Appl Environ Microbiol, 63, pp. 2884-2896
  • Sokal, R.R., Rohlf, F.J., (1995) Biometry: The Principles and Practice of Statistics in Biological Research., , New York, NY, USA: New York W.H. Freeman
  • Suzuki, M.T., Giovannoni, S.J., Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR (1996) Appl Environ Microbiol, 62, pp. 625-630
  • Thompson, J.R., Marcelino, L.A., Polz, M.F., Heteroduplexes in mixed-template amplifications: Formation, consequence and elimination by 'reconditioning PCR' (2002) Nucleic Acids Res, 30, pp. 2083-2088
  • Thomsen, T.R., Nielsen, J.L., Ramsing, N.B., Nielsen, P.H., Micromanipulation and further identification of FISH-labelled microcolonies of a dominant denitrifying bacterium in activated sludge (2004) Environ Microbiol, 6, pp. 470-479
  • Tokeshi, M., Niche apportionment or random assortment: Species abundance patterns revisited (1990) J Anim Ecol, 59, pp. 1129-1146
  • Tokeshi, M., Species abundance patterns and community structure (1993) Adv Ecol Res, 24, pp. 111-186
  • Wagner, M., Amann, R., Kampfer, P., Assmus, B., Hartmann, A., Hutzler, P., Identification and in situ detection of Gram-negative filamentous bacteria in activated sludge (1994) Syst Appl Microbiol, 17, pp. 405-417
  • Wagner, M., Loy, A., Nogueira, R., Purkhold, U., Lee, N., Daims, H., Microbial community composition and function in wastewater treatment plants (2002) Antonie Van Leeuwenhoek, 81, pp. 665-680
  • Wallner, G., Amann, R., Beisker, W., Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms (1993) Cytometry, 14, pp. 136-143
  • Yilmaz, L.S., Okten, H.E., Noguera, D.R., Making all parts of the 16S rRNA of Escherichia coli accessible in situ to single DNA oligonucleotides (2006) Appl Environ Microbiol, 72, pp. 733-744


---------- APA ----------
Figuerola, E.L.M. & Erijman, L. (2007) . Bacterial taxa abundance pattern in an industrial wastewater treatment system determined by the full rRNA cycle approach. Environmental Microbiology, 9(7), 1780-1789.
---------- CHICAGO ----------
Figuerola, E.L.M., Erijman, L. "Bacterial taxa abundance pattern in an industrial wastewater treatment system determined by the full rRNA cycle approach" . Environmental Microbiology 9, no. 7 (2007) : 1780-1789.
---------- MLA ----------
Figuerola, E.L.M., Erijman, L. "Bacterial taxa abundance pattern in an industrial wastewater treatment system determined by the full rRNA cycle approach" . Environmental Microbiology, vol. 9, no. 7, 2007, pp. 1780-1789.
---------- VANCOUVER ----------
Figuerola, E.L.M., Erijman, L. Bacterial taxa abundance pattern in an industrial wastewater treatment system determined by the full rRNA cycle approach. Environ. Microbiol. 2007;9(7):1780-1789.