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Divergence And Redundancy Of 16S RRNA Sequences In Genomes With Multiple Rrn Operons.
S. Acinas, L. Marcelino, V. Klepac-Ceraj, M. Polz
Published 2004 · Biology, Medicine
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The level of sequence heterogeneity among rrn operons within genomes determines the accuracy of diversity estimation by 16S rRNA-based methods. Furthermore, the occurrence of widespread horizontal gene transfer (HGT) between distantly related rrn operons casts doubt on reconstructions of phylogenetic relationships. For this study, patterns of distribution of rrn copy numbers, interoperonic divergence, and redundancy of 16S rRNA sequences were evaluated. Bacterial genomes display up to 15 operons and operon numbers up to 7 are commonly found, but approximately 40% of the organisms analyzed have either one or two operons. Among the Archaea, a single operon appears to dominate and the highest number of operons is five. About 40% of sequences among 380 operons in 76 bacterial genomes with multiple operons were identical to at least one other 16S rRNA sequence in the same genome, and in 38% of the genomes all 16S rRNAs were invariant. For Archaea, the number of identical operons was only 25%, but only five genomes with 21 operons are currently available. These considerations suggest an upper bound of roughly threefold overestimation of bacterial diversity resulting from cloning and sequencing of 16S rRNA genes from the environment; however, the inclusion of genomes with a single rrn operon may lower this correction factor to approximately 2.5. Divergence among operons appears to be small overall for both Bacteria and Archaea, with the vast majority of 16S rRNA sequences showing <1% nucleotide differences. Only five genomes with operons with a higher level of nucleotide divergence were detected, and Thermoanaerobacter tengcongensis exhibited the highest level of divergence (11.6%) noted to date. Overall, four of the five extreme cases of operon differences occurred among thermophilic bacteria, suggesting a much higher incidence of HGT in these bacteria than in other groups.
This paper references
A complete sequence of the T. tengcongensis genome.
Q. Bao (2002)
Prokaryotic Diversity--Magnitude, Dynamics, and Controlling Factors
V. Torsvik (2002)
Cultivation of the ubiquitous SAR11 marine bacterioplankton clade
M. Rappé (2002)
High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria.
V. Klepac-Ceraj (2004)
Prokaryotic Genome Size and SSU rDNA Copy Number: Estimation of Microbial Relative Abundance from a Mixed Population
G. Fogel (1999)
Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity.
L. D. Crosby (2003)
Horizontal gene transfer among genomes: the complexity hypothesis.
R. Jain (1999)
Multiple sequence alignment with Clustal X.
F. Jeanmougin (1998)
Counting the Uncountable: Statistical Approaches to Estimating Microbial Diversity
J. B. Hughes (2001)
Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria.
K. Field (1997)
Variable numbers of rRNA gene operons in Bacillus cereus strains.
T. Johansen (1996)
Phylogenetics and the Cohesion of Bacterial Genomes
V. Daubin (2003)
Thermoanaerobacter tengcongensis sp. nov., a novel anaerobic, saccharolytic, thermophilic bacterium isolated from a hot spring in Tengcong, China.
Y. Xue (2001)
rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria
J. A. Klappenbach (2000)
Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis
N. Ivanova (2003)
Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics.
D. Smith (1997)
Suppressive subtractive hybridization detects extensive genomic diversity in Thermotoga maritima.
C. Nesbø (2002)
Microbial Evolution, Diversity, and Ecology: A Decade of Ribosomal RNA Analysis of Uncultivated Microorganisms
I. Head (1998)
rrndb: the Ribosomal RNA Operon Copy Number Database
J. A. Klappenbach (2001)
Evidence for biased gene conversion in concerted evolution of ribosomal DNA.
D. Hillis (1991)
High genetic and physiological diversity of sulfate-reducing bacteria isolated from an oligotrophic lake sediment
H. Sass (1998)
Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation
G. Rocap (2003)
16S rRNAs IN GENOMES WITH MULTIPLE rrn OPERONS
Multiple sequence alignment with ClustalX
F Jeanmougin (1998)
Corrections: The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus
H. Klenk (1998)
Two different 16S rRNA genes in a mycobacterial strain.
B. Ninet (1996)
16S rRNA Sequence Diversity in Mycobacterium celatum Strains Caused by Presence of Two Different Copies of 16S rRNA Gene
U. Reischl (1998)
rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation.
C. Condon (1995)
Estimating prokaryotic diversity and its limits
T. Curtis (2002)
How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity.
G. Fox (1992)
Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides.
S. C. Dryden (1990)
The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes.
Y. Wang (1997)
Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui.
S. Mylvaganam (1992)
Microheterogeneity in 16S Ribosomal DNA-Defined Bacterial Populations from a Stratified Planktonic Environment Is Related to Temporal Changes and to Ecological Adaptations
E. O. Casamayor (2002)
Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori
R. Alm (1999)
Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity.
P. Hugenholtz (1998)
Heterogeneity of the Nucleotide Sequences of the 16S rRNA Genes of the Type Strain of Desulfotomaculum kuznetsovii
T. P. Tourova (2004)
Sequence heterogeneity of the ten rRNA operons in Clostridium perfringens.
T. Shimizu (2001)
Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group I
J. García-Martínez (2000)
The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus
Hans-Peter Klenk (1997)
Correlation of 16S ribosomal DNA signature sequences with temperature-dependent growth rates of mesophilic and psychrotolerant strains of the Bacillus cereus group.
B. Prüß (1999)
Gene Conversion Drives Within Genic Sequences: Concerted Evolution of Ribosomal RNA Genes in Bacteria and Archaea
D. Liao (2000)
Distinct types of rRNA operons exist in the genome of the actinomycete Thermomonospora chromogena and evidence for horizontal transfer of an entire rRNA operon.
W. H. Yap (1999)
Genome evolution at the genus level: comparison of three complete genomes of hyperthermophilic archaea.
O. Lecompte (2001)
Concerted evolution: molecular mechanism and biological implications.
D. Liao (1999)
Genome sequence of enterohaemorrhagic Escherichia coli O157:H7
Nicole T. Perna (2001)
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Ecosystem Ecology and Geochemistry of Cuatro Cienegas
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