Nucleic Acids Research, 2001, Vol. 29, No. 1 181-184
© 2001 Oxford University Press
rrndb: the Ribosomal RNA Operon Copy Number Database
1Department of Microbiology and Molecular Genetics and 2Center for Microbial Ecology, Michigan State University, 203 Giltner Hall, East Lansing, MI 48824-1101, USA
Received August 30, 2000; Revised and Accepted October 25, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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The Ribosomal RNA Operon Copy Number Database (rrndb) is an Internet-accessible database containing annotated information on rRNA operon copy number among prokaryotes. Gene redundancy is uncommon in prokaryotic genomes, yet the rRNA genes can vary from one to as many as 15 copies. Despite the widespread use of 16S rRNA gene sequences for identification of prokaryotes, information on the number and sequence of individual rRNA genes in a genome is not readily accessible. In an attempt to understand the evolutionary implications of rRNA operon redundancy, we have created a phylogenetically arranged report on rRNA gene copy number for a diverse collection of prokaryotic microorganisms. Each entry (organism) in the rrndb contains detailed information linked directly to external websites including the Ribosomal Database Project, GenBank, PubMed and several culture collections. Data contained in the rrndb will be valuable to researchers investigating microbial ecology and evolution using 16S rRNA gene sequences. The rrndb web site is directly accessible on the WWW at http://rrndb.cme.msu.edu.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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Microbes are the most abundant and most diverse forms of life on earth (1). Despite their ubiquity, it is clear that only a small percentage of microbes (0.1–0.5%) has been cultivated in the laboratory (2). Identification and classification of microbes is further confounded by a general absence of morphologically distinct features—thousands of bacterial species can be categorized by a few different (
17) morphologies. For the past 10–15 years, microbiologists have relied upon DNA sequence information for microbial identification, based primarily on the genes encoding the small subunit RNA molecule of the ribosome (16S rRNA or SSU rRNA). Functional constraints on the translational apparatus limit variability in the 16S rRNA molecule, resulting in a high degree of sequence conservation. The conservation of the rRNA gene sequence permits bacterial characterization based on sequence information obtained from pure cultures or cloned genes from mixed communities. A priori knowledge of rRNA sequence data can be used to design phylogenetically conserved probes that target both individual and closely related groups of microorganisms without cultivation. A principle repository of 16S rRNA sequences, the Ribosomal Database Project, currently maintains over 17 000 aligned entries (12 425 sequences 
900 bp) representing 850 of 940 formally recognized prokaryotic genera, which are placed into 1149 phylogenetic groups (3). The ribosomal RNA genes (encoding 16S, 23S and 5S rRNAs) are typically linked together with tRNA molecules into operons that are coordinately transcribed to produce equimolar quantities of each gene product. During rapid exponential growth (µ = 2.5 h–1), the effective number of rRNA operons in Escherichia coli can be as high as 36 copies (4). Sequence heterogeneity exists among multiple rRNA genes encoded on a single genome, yet little evidence exists suggesting functional independence (5,6). While reports of intra-genomic variability of 16S rRNA range as high as 6.5% (7), an analysis of complete genome sequences stored in the rrndb indicates a maximum of 1.23% (E.coli) among the 14 species examined (Table 1). Both rRNA operon redundancy and intra-genomic sequence heterogeneity have important practical implications for researchers attempting to identify and quantify bacteria using rRNA sequence data (8,9).
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Molecular methods for microbial diversity assessment rely primarily on PCR-amplification of 16S rRNA genes from complex samples followed by (i) cloning and sequencing of unique amplicons, (ii) separation of amplicons based on chemical composition via denaturing- or temperature-gradient gel electrophoresis (10,11), or (iii) separation of amplicons after restriction digestion based on size via terminal restriction fragment length polymorphism analysis (12). The number of unique sequences or bands detected by these methods is often considered a proxy for organismal diversity. Rather, due to intra-genomic 16S rRNA heterogeneity, these methods are more accurately a measure of 16S rRNA sequence diversity. Similarly, intra-genomic sequence heterogeneity limits the phylogenetic resolution of the 16S rRNA gene (13,14). The majority of 16S rRNA entries in public databases, such as GenBank and the Ribosomal Database Project, are ‘composite’ sequences obtained from sequencing PCR amplicons generated through simultaneous amplification of all 16S rRNA gene copies on a genome (15).
In an attempt to understand the evolutionary implications of rRNA operon gene redundancy, our laboratory has maintained an internal database of rRNA operon copy number values for both Bacteria and Archaea. Mapping of this information onto a phylogenetic tree indicates that phylogenetic relatedness is not the sole determinant of rRNA operon copy number (16). Rather, bacteria with the same number of rRNA operons appear to have arisen convergently in several phylogenetic lineages. While our primary interest resides in elucidating the underlying physiological and evolutionary consequences of rRNA operon multiplicity, rRNA operon copy number information has become increasingly valuable to researchers performing emerging technologies such as quantitative real-time PCR (17). Working closely with the Ribosomal Database Project at Michigan State University, we have created an Internet-based interactive database of rRNA operon copy number values for a diverse collection prokaryotic microorganisms: The Ribosomal RNA Operon Copy Number Database (rrndb).
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DATABASE DESCRIPTION |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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The rrndb provides information pertaining to the number of rRNA operons contained on the genomes of prokaryotic microorganisms in a phylogenetic context. The rrndb is co-located with the RDP server at the Center for Microbial Ecology at Michigan State University and is accessible via the WWW at http://rrndb.cme.msu.edu. The initial release of our database (December, 2000) contains over 250 annotated entries, including information from all full-genome sequencing projects completed at the time of release. An internal database management system (described below) permits entry of data from any WWW browser, facilitating public release of information shortly after entry and verification. The rrndb WWW site also contains answers to frequently asked questions, an opportunity to provide feedback and a form for direct submission of new data.
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WEB INTERFACE |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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Information contained within the rrndb is accessible via three main interfaces: (i) ‘Operon Sort’, a complete list of organisms in the database presented in alphabetical order; (ii) ‘Phylo Sort’, rRNA operon copy number mapped onto the RDP organismal hierarchy; and (iii) a ‘Search’ page. The ‘Operon Sort’ list can be sorted in ascending and descending order by organism name, rRNA operon copy number or genome size (Fig. 1A). rRNA operon copy number is mapped onto the RDP organismal hierarchy presented on the ‘Phylo Sort’ page. The hierarchy is expandable and collapsible and mean rRNA operon copy number is displayed for each phylogenetic group (Fig. 1B). User queries can be entered on the ‘Search’ page, which also offers advanced searches limited to rRNA operon copy number and genome size. Each entry in the rrndb is linked to an individual page containing detailed information about the selected organism, including: genus, species, sub-species, strain, culture deposit, 16S, 23S and 5S rRNA gene copy number, phylogenetic position, genome size, genome sequence availability, 16S rRNA sequence records and literature reference(s). Sequence deposits are linked directly to GenBank and the RDP, culture deposits to the American Type Culture Collection (ATCC) and Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ) and references to the National Library of Medicine’s PubMed database. 16S rRNA genes from individual rRNA operons are denoted when available and include gene start and stop locations within GenBank entries from full-genome sequence deposits.
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DATA CURATION |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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All entries in the rrndb possess at least a genus name, strain designation or culture deposit number and a literature or electronic reference describing rRNA operon copy number determination. The entries for each organism are obtained from computerized searches of reference databases (PubMed, ISI Current Contents, etc.), literature articles, full genome sequencing projects listed at The Institute for Genomic Research (http://www.tigr.org) and the National Center for Biotechnology Information’s web sites (http://www.ncbi.nlm.nih.gov) and from direct web site submission. Effort is made to include all pertinent references to the determination of rRNA operon copy number for an organism. Literature references for a particular organism may not be reported due to an article predating electronic database records or to the absence of relevant search terms in a database entry. If the complete genome sequence of an organism is available, those data are considered to be the most accurate determination of rRNA operon copy number and is the only reported reference. In certain instances the 16S, 23S and 5S rRNA genes are not present in equal numbers per genome (18). Laboratory methods to determine rRNA operon copy number typically rely upon Southern hybridization of a 16S rRNA-based probe to restriction-digested genomic DNA; in these instances, the number of 16S rRNA genes serves as an estimate for rRNA operon copy number.
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DATABASE MANAGEMENT SYSTEM |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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The rrndb data are stored using the MySQL relational database management system (RDBMS), which supports the structured query language (SQL) standard (http://www.mysql.com). The WWW interface to the rrndb is generated by Java Server Pages and Java Servlets that retrieve information to be displayed by employing custom designed JavaBean objects (http://java.sun.com). These objects access the database using MM MySQL JDBC drivers (http://www.worldserver.com/mm.mysql). The rrndb website is hosted on a Sun Ultra 60 server running the Solaris 2.6 operating system and Apache Software Foundation’s Apache HTTP and Tomcat servers (http://jakarta.apache.org).
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FUTURE CHANGES AND ADDITIONS |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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Planned additions to the rrndb include interface tools to select and download individual organism entries from both the ‘Operon Sort’ list and the ‘Phylo Sort’ pages. Information on intra-genomic rRNA sequence variability, such as presented in Table 1, will be added for organisms with full genome sequences. Further changes will be dictated by feedback obtained from users of the rrndb website. It is anticipated that the rrndb will be updated on a quarterly basis as new information becomes available through electronic databases and full-genome sequencing projects.
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ACKNOWLEDGEMENTS |
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We thank C. T. Parker and J. M. Stredwick for early prototype development and hardware support for the rrndb. Funds provided by the National Science Foundation (IBN-9875254), the Center for Microbial Ecology at Michigan State University (BIR91-20006) and the US Department of Energy (to the RDP) supported the development of the rrndb.
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FOOTNOTES |
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* To whom correspondence should be addressed at: Department of Microbiology and Molecular Genetics, Michigan State University, 202 Giltner Hall, East Lansing, MI 48824-1101, USA. Tel: +1 517 353 1796; Fax: +1 517 353 8957; Email: tschmidt{at}msu.edu
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REFERENCES |
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TOPABSTRACTINTRODUCTIONDATABASE DESCRIPTIONWEB INTERFACEDATA CURATIONDATABASE MANAGEMENT SYSTEMFUTURE CHANGES AND ADDITIONSREFERENCES |
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R. Danovaro, G. M. Luna, A. Dell'Anno, and B. Pietrangeli Comparison of Two Fingerprinting Techniques, Terminal Restriction Fragment Length Polymorphism and Automated Ribosomal Intergenic Spacer Analysis, for Determination of Bacterial Diversity in Aquatic Environments Appl. Envir. Microbiol., September 1, 2006; 72(9): 5982 - 5989. [Abstract] [Full Text] [PDF]
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 H. Sokol, P. Lepage, P. Seksik, J. Dore, and P. Marteau Temperature Gradient Gel Electrophoresis of Fecal 16S rRNA Reveals Active Escherichia coli in the Microbiota of Patients with Ulcerative Colitis. J. Clin. Microbiol., September 1, 2006; 44(9): 3172 - 3177. [Abstract] [Full Text] [PDF]
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D. L. Bedard, J. J. Bailey, B. L. Reiss, and G. V. S. Jerzak Development and Characterization of Stable Sediment-Free Anaerobic Bacterial Enrichment Cultures That Dechlorinate Aroclor 1260 Appl. Envir. Microbiol., April 1, 2006; 72(4): 2460 - 2470. [Abstract] [Full Text] [PDF]
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M. Webber, A. M. Buckley, L. P. Randall, M. J. Woodward, and L. J. V. Piddock Overexpression of marA, soxS and acrB in veterinary isolates of Salmonella enterica rarely correlates with cyclohexane tolerance J. Antimicrob. Chemother., April 1, 2006; 57(4): 673 - 679. [Abstract] [Full Text] [PDF]
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C. Palmer, E. M. Bik, M. B. Eisen, P. B. Eckburg, T. R. Sana, P. K. Wolber, D. A. Relman, and P. O. Brown Rapid quantitative profiling of complex microbial populations Nucleic Acids Res., January 10, 2006; 34(1): e5 - e5. [Abstract] [Full Text] [PDF]
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H. Penning and R. Conrad Effect of Inhibition of Acetoclastic Methanogenesis on Growth of Archaeal Populations in an Anoxic Model Environment Appl. Envir. Microbiol., January 1, 2006; 72(1): 178 - 184. [Abstract] [Full Text] [PDF]
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C. W. M. Geraats-Peters, M. Brouwers, P. M. Schneeberger, A. G. M. van der Zanden, S. M. Bruisten, G. Weers-Pothoff, C. H. E. Boel, A. J. C. van den Brule, H. G. Harmsen, and M. H. A. Hermans Specific and Sensitive Detection of Neisseria gonorrhoeae in Clinical Specimens by Real-Time PCR J. Clin. Microbiol., November 1, 2005; 43(11): 5653 - 5659. [Abstract] [Full Text] [PDF]
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A. V. Karlyshev and B. W. Wren Development and Application of an Insertional System for Gene Delivery and Expression in Campylobacter jejuni Appl. Envir. Microbiol., July 1, 2005; 71(7): 4004 - 4013. [Abstract] [Full Text] [PDF]
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N. Fierer, J. A. Jackson, R. Vilgalys, and R. B. Jackson Assessment of Soil Microbial Community Structure by Use of Taxon-Specific Quantitative PCR Assays Appl. Envir. Microbiol., July 1, 2005; 71(7): 4117 - 4120. [Abstract] [Full Text] [PDF]
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C. R. Osorio, M. D. Collins, J. L. Romalde, and A. E. Toranzo Variation in 16S-23S rRNA Intergenic Spacer Regions in Photobacterium damselae: a Mosaic-Like Structure Appl. Envir. Microbiol., February 1, 2005; 71(2): 636 - 645. [Abstract] [Full Text] [PDF]
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P. V. Dunlap and J. C. Ast Genomic and Phylogenetic Characterization of Luminous Bacteria Symbiotic with the Deep-Sea Fish Chlorophthalmus albatrossis (Aulopiformes: Chlorophthalmidae) Appl. Envir. Microbiol., February 1, 2005; 71(2): 930 - 939. [Abstract] [Full Text] [PDF]
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B. S. Stevenson and T. M. Schmidt Life History Implications of rRNA Gene Copy Number in Escherichia coli Appl. Envir. Microbiol., November 1, 2004; 70(11): 6670 - 6677. [Abstract] [Full Text] [PDF]
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M. Cardinale, L. Brusetti, P. Quatrini, S. Borin, A. M. Puglia, A. Rizzi, E. Zanardini, C. Sorlini, C. Corselli, and D. Daffonchio Comparison of Different Primer Sets for Use in Automated Ribosomal Intergenic Spacer Analysis of Complex Bacterial Communities Appl. Envir. Microbiol., October 1, 2004; 70(10): 6147 - 6156. [Abstract] [Full Text] [PDF]
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 O. Norkina, T. G. Burnett, and R. C. De Lisle Bacterial Overgrowth in the Cystic Fibrosis Transmembrane Conductance Regulator Null Mouse Small Intestine Infect. Immun., October 1, 2004; 72(10): 6040 - 6049. [Abstract] [Full Text] [PDF]
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V. G. Meka, H. S. Gold, A. Cooke, L. Venkataraman, G. M. Eliopoulos, R. C. Moellering Jr, and S. G. Jenkins Reversion to susceptibility in a linezolid-resistant clinical isolate of Staphylococcus aureus J. Antimicrob. Chemother., October 1, 2004; 54(4): 818 - 820. [Abstract] [Full Text] [PDF]
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M. Labrenz, I. Brettar, R. Christen, S. Flavier, J. Botel, and M. G. Hofle Development and Application of a Real-Time PCR Approach for Quantification of Uncultured Bacteria in the Central Baltic Sea Appl. Envir. Microbiol., August 1, 2004; 70(8): 4971 - 4979. [Abstract] [Full Text] [PDF]
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J. R. Thompson, M. A. Randa, L. A. Marcelino, A. Tomita-Mitchell, E. Lim, and M. F. Polz Diversity and Dynamics of a North Atlantic Coastal Vibrio Community Appl. Envir. Microbiol., July 1, 2004; 70(7): 4103 - 4110. [Abstract] [Full Text] [PDF]
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S. Bartosch, A. Fite, G. T. Macfarlane, and M. E. T. McMurdo Characterization of Bacterial Communities in Feces from Healthy Elderly Volunteers and Hospitalized Elderly Patients by Using Real-Time PCR and Effects of Antibiotic Treatment on the Fecal Microbiota Appl. Envir. Microbiol., June 1, 2004; 70(6): 3575 - 3581. [Abstract] [Full Text] [PDF]
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 S. Nandi, J. J. Maurer, C. Hofacre, and A. O. Summers Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter PNAS, May 4, 2004; 101(18): 7118 - 7122. [Abstract] [Full Text] [PDF]
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R. B. Sarma-Rupavtarm, Z. Ge, D. B. Schauer, J. G. Fox, and M. F. Polz Spatial Distribution and Stability of the Eight Microbial Species of the Altered Schaedler Flora in the Mouse Gastrointestinal Tract Appl. Envir. Microbiol., May 1, 2004; 70(5): 2791 - 2800. [Abstract] [Full Text] [PDF]
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S. G. Acinas, L. A. Marcelino, V. Klepac-Ceraj, and M. F. Polz Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons J. Bacteriol., May 1, 2004; 186(9): 2629 - 2635. [Abstract] [Full Text] [PDF]
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 D. W. Ussery, P. F. Hallin, K. Lagesen, and T. Coenye Genome Update: rRNAs in sequenced microbial genomes Microbiology, May 1, 2004; 150(5): 1113 - 1115. [Full Text] [PDF]
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N. M. E. J. Leys, A. Ryngaert, L. Bastiaens, W. Verstraete, E. M. Top, and D. Springael Occurrence and Phylogenetic Diversity of Sphingomonas Strains in Soils Contaminated with Polycyclic Aromatic Hydrocarbons Appl. Envir. Microbiol., April 1, 2004; 70(4): 1944 - 1955. [Abstract] [Full Text] [PDF]
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G. D. Inglis and L. D. Kalischuk Direct Quantification of Campylobacter jejuni and Campylobacter lanienae in Feces of Cattle by Real-Time Quantitative PCR Appl. Envir. Microbiol., April 1, 2004; 70(4): 2296 - 2306. [Abstract] [Full Text] [PDF]
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T. L. Skovhus, N. B. Ramsing, C. Holmstrom, S. Kjelleberg, and I. Dahllof Real-Time Quantitative PCR for Assessment of Abundance of Pseudoalteromonas Species in Marine Samples Appl. Envir. Microbiol., April 1, 2004; 70(4): 2373 - 2382. [Abstract] [Full Text] [PDF]
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J. R. Graber, J. R. Leadbetter, and J. A. Breznak Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the First Spirochetes Isolated from Termite Guts Appl. Envir. Microbiol., March 1, 2004; 70(3): 1315 - 1320. [Abstract] [Full Text] [PDF]
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H. M. Dionisi, G. Harms, A. C. Layton, I. R. Gregory, J. Parker, S. A. Hawkins, K. G. Robinson, and G. S. Sayler Power Analysis for Real-Time PCR Quantification of Genes in Activated Sludge and Analysis of the Variability Introduced by DNA Extraction Appl. Envir. Microbiol., November 1, 2003; 69(11): 6597 - 6604. [Abstract] [Full Text] [PDF]
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P. P. Sheridan, V. I. Miteva, and J. E. Brenchley Phylogenetic Analysis of Anaerobic Psychrophilic Enrichment Cultures Obtained from a Greenland Glacier Ice Core Appl. Envir. Microbiol., April 1, 2003; 69(4): 2153 - 2160. [Abstract] [Full Text] [PDF]
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J. G. Hashimoto, B. S. Stevenson, and T. M. Schmidt Rates and Consequences of Recombination between rRNA Operons J. Bacteriol., February 1, 2003; 185(3): 966 - 972. [Abstract] [Full Text] [PDF]
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D. L. Distel, D. J. Beaudoin, and W. Morrill Coexistence of Multiple Proteobacterial Endosymbionts in the Gills of the Wood-Boring Bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae) Appl. Envir. Microbiol., December 1, 2002; 68(12): 6292 - 6299. [Abstract] [Full Text] [PDF]
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E. Barbieri, G. Riccioni, A. Pisano, D. Sisti, S. Zeppa, D. Agostini, and V. Stocchi Competitive PCR for Quantitation of a Cytophaga-Flexibacter-Bacteroides Phylum Bacterium Associated with the Tuber borchii Vittad. Mycelium Appl. Envir. Microbiol., December 1, 2002; 68(12): 6421 - 6424. [Abstract] [Full Text] [PDF]
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A. Kaetzke and K. Eschrich Simultaneous determination of different DNA sequences by mass spectrometric evaluation of Sanger sequencing reactions Nucleic Acids Res., November 1, 2002; 30(21): e117 - e117. [Abstract] [Full Text] [PDF]
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T. D. Leser, J. Z. Amenuvor, T. K. Jensen, R. H. Lindecrona, M. Boye, and K. Moller Culture-Independent Analysis of Gut Bacteria: the Pig Gastrointestinal Tract Microbiota Revisited Appl. Envir. Microbiol., February 1, 2002; 68(2): 673 - 690. [Abstract] [Full Text] [PDF]
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H. M. Dionisi, A. C. Layton, G. Harms, I. R. Gregory, K. G. Robinson, and G. S. Sayler Quantification of Nitrosomonas oligotropha-Like Ammonia-Oxidizing Bacteria and Nitrospira spp. from Full-Scale Wastewater Treatment Plants by Competitive PCR Appl. Envir. Microbiol., January 1, 2002; 68(1): 245 - 253. [Abstract] [Full Text] [PDF]
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B. L. Maidak, J. R. Cole, T. G. Lilburn, C. T. Parker Jr, P. R. Saxman, R. J. Farris, G. M. Garrity, G. J. Olsen, T. M. Schmidt, and J. M. Tiedje The RDP-II (Ribosomal Database Project) Nucleic Acids Res., January 1, 2001; 29(1): 173 - 174. [Abstract] [Full Text] [PDF]
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