Marker genes that are less conserved in their sequences are useful for predicting genome-wide similarity levels between closely related prokaryotic strains
Abstract
The 16s rRNA gene is so far the most widely used marker for taxonomical classification and separation of prokaryotes. Since it is universally conserved among prokaryotes, it is possible to use this gene to classify a broad range of prokaryotic organisms. At the same time, it has often been noted that the 16s rRNA gene is too conserved to separate between prokaryotes at finer taxonomic levels. In this paper, we examine how well levels of similarity of 16s rRNA and 73 additional universal or nearly universal marker genes correlate with genome-wide levels of gene sequence similarity. We demonstrate that the percent identity of 16s rRNA predicts genome-wide levels of similarity very well for distantly related prokaryotes, but not for closely related ones. In closely related prokaryotes, we find that there are many other marker genes for which levels of similarity are much more predictive of genome-wide levels of gene sequence similarity. Finally, we show that the identities of the markers that are most useful for predicting genome-wide levels of similarity within closely related prokaryotic lineages vary greatly between lineages. However, the most useful markers are always those that are least conserved in their sequences within each lineage. In conclusion, ourmore »
- Authors:
- Publication Date:
- Research Org.:
- Drexel Univ., Philadelphia, PA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1618942
- Alternate Identifier(s):
- OSTI ID: 1282888
- Grant/Contract Number:
- SC0004335
- Resource Type:
- Published Article
- Journal Name:
- Microbiome
- Additional Journal Information:
- Journal Name: Microbiome Journal Volume: 4 Journal Issue: 1; Journal ID: ISSN 2049-2618
- Publisher:
- Springer Science + Business Media
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Less-conserved genes; Lineage-specific; Marker genes; Genome-wide similarity; ribosomal-rna gene; microbial communities; gut microbiome; database; diversity; bacterial; metagenomics; reconstruction; identification; accurate
Citation Formats
Lan, Yemin, Rosen, Gail, and Hershberg, Ruth. Marker genes that are less conserved in their sequences are useful for predicting genome-wide similarity levels between closely related prokaryotic strains. United Kingdom: N. p., 2016.
Web. doi:10.1186/s40168-016-0162-5.
Lan, Yemin, Rosen, Gail, & Hershberg, Ruth. Marker genes that are less conserved in their sequences are useful for predicting genome-wide similarity levels between closely related prokaryotic strains. United Kingdom. https://doi.org/10.1186/s40168-016-0162-5
Lan, Yemin, Rosen, Gail, and Hershberg, Ruth. Tue .
"Marker genes that are less conserved in their sequences are useful for predicting genome-wide similarity levels between closely related prokaryotic strains". United Kingdom. https://doi.org/10.1186/s40168-016-0162-5.
@article{osti_1618942,
title = {Marker genes that are less conserved in their sequences are useful for predicting genome-wide similarity levels between closely related prokaryotic strains},
author = {Lan, Yemin and Rosen, Gail and Hershberg, Ruth},
abstractNote = {The 16s rRNA gene is so far the most widely used marker for taxonomical classification and separation of prokaryotes. Since it is universally conserved among prokaryotes, it is possible to use this gene to classify a broad range of prokaryotic organisms. At the same time, it has often been noted that the 16s rRNA gene is too conserved to separate between prokaryotes at finer taxonomic levels. In this paper, we examine how well levels of similarity of 16s rRNA and 73 additional universal or nearly universal marker genes correlate with genome-wide levels of gene sequence similarity. We demonstrate that the percent identity of 16s rRNA predicts genome-wide levels of similarity very well for distantly related prokaryotes, but not for closely related ones. In closely related prokaryotes, we find that there are many other marker genes for which levels of similarity are much more predictive of genome-wide levels of gene sequence similarity. Finally, we show that the identities of the markers that are most useful for predicting genome-wide levels of similarity within closely related prokaryotic lineages vary greatly between lineages. However, the most useful markers are always those that are least conserved in their sequences within each lineage. In conclusion, our results show that by choosing markers that are less conserved in their sequences within a lineage of interest, it is possible to better predict genome-wide gene sequence similarity between closely related prokaryotes than is possible using the 16s rRNA gene. We point readers towards a database we have created (POGO-DB) that can be used to easily establish which markers show lowest levels of sequence conservation within different prokaryotic lineages.},
doi = {10.1186/s40168-016-0162-5},
journal = {Microbiome},
number = 1,
volume = 4,
place = {United Kingdom},
year = {Tue May 03 00:00:00 EDT 2016},
month = {Tue May 03 00:00:00 EDT 2016}
}
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https://doi.org/10.1186/s40168-016-0162-5
https://doi.org/10.1186/s40168-016-0162-5
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Cited by: 42 works
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Figures / Tables:
Fig. 1: Box and whisker plot of 16s rRNA percent identities between genomes of the same taxa (species/genus/etc.). The whiskers represent boundaries within 1.5 interquartile range of the lower and upper quartiles. Although the 16s rRNA genes are more similar at finer taxonomic levels, there are still large overlaps betweenmore »
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Works referenced in this record:
Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data
journal, October 2013
- Eren, A. Murat; Maignien, Loïs; Sul, Woo Jun
- Methods in Ecology and Evolution, Vol. 4, Issue 12
Enterotypes of the human gut microbiome
journal, April 2011
- Arumugam, Manimozhiyan; Raes, Jeroen; Pelletier, Eric
- Nature, Vol. 473, Issue 7346
Phylogenomic analysis of bacterial and archaeal sequences with AMPHORA2
journal, February 2012
- Wu, Martin; Scott, Alexandra J.
- Bioinformatics, Vol. 28, Issue 7
Metagenomics: Genomic Analysis of Microbial Communities
journal, December 2004
- Riesenfeld, Christian S.; Schloss, Patrick D.; Handelsman, Jo
- Annual Review of Genetics, Vol. 38, Issue 1
The Human Microbiome Project: A Community Resource for the Healthy Human Microbiome
journal, August 2012
- Gevers, Dirk; Knight, Rob; Petrosino, Joseph F.
- PLoS Biology, Vol. 10, Issue 8
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006
- DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
- Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
The Variability of the 16S rRNA Gene in Bacterial Genomes and Its Consequences for Bacterial Community Analyses
journal, February 2013
- Větrovský, Tomáš; Baldrian, Petr
- PLoS ONE, Vol. 8, Issue 2
A Comparison of rpoB and 16S rRNA as Markers in Pyrosequencing Studies of Bacterial Diversity
journal, February 2012
- Vos, Michiel; Quince, Christopher; Pijl, Agata S.
- PLoS ONE, Vol. 7, Issue 2
Identification of common molecular subsequences
journal, March 1981
- Smith, T. F.; Waterman, M. S.
- Journal of Molecular Biology, Vol. 147, Issue 1, p. 195-197
Using the Basic Local Alignment Search Tool (BLAST)
journal, July 2007
- Mount, David W.
- Cold Spring Harbor Protocols, Vol. 2007, Issue 7
TOPD/FMTS: a new software to compare phylogenetic trees
journal, April 2007
- Puigbo, P.; Garcia-Vallve, S.; McInerney, J. O.
- Bioinformatics, Vol. 23, Issue 12
Assessing diversity of the female urine microbiota by high throughput sequencing of 16S rDNA amplicons
journal, January 2011
- Siddiqui, Huma; Nederbragt, Alexander J.; Lagesen, Karin
- BMC Microbiology, Vol. 11, Issue 1
Deep Sequencing of the Oral Microbiome Reveals Signatures of Periodontal Disease
journal, June 2012
- Liu, Bo; Faller, Lina L.; Klitgord, Niels
- PLoS ONE, Vol. 7, Issue 6
cpnDB: A Chaperonin Sequence Database
journal, August 2004
- Hill, J. E.
- Genome Research, Vol. 14, Issue 8
Simultaneous Amplicon Sequencing to Explore Co-Occurrence Patterns of Bacterial, Archaeal and Eukaryotic Microorganisms in Rumen Microbial Communities
journal, February 2013
- Kittelmann, Sandra; Seedorf, Henning; Walters, William A.
- PLoS ONE, Vol. 8, Issue 2
Toward Automatic Reconstruction of a Highly Resolved Tree of Life
journal, March 2006
- Ciccarelli, F. D.
- Science, Vol. 311, Issue 5765
Species Identification and Profiling of Complex Microbial Communities Using Shotgun Illumina Sequencing of 16S rRNA Amplicon Sequences
journal, April 2013
- Ong, Swee Hoe; Kukkillaya, Vinutha Uppoor; Wilm, Andreas
- PLoS ONE, Vol. 8, Issue 4
A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010
- Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
- Nature, Vol. 464, Issue 7285
Predicting relatedness of bacterial genomes using the chaperonin-60 universal target (cpn60 UT): Application to Thermoanaerobacter species
journal, May 2011
- Verbeke, Tobin J.; Sparling, Richard; Hill, Janet E.
- Systematic and Applied Microbiology, Vol. 34, Issue 3
Bioinformatics for Whole-Genome Shotgun Sequencing of Microbial Communities
journal, January 2005
- Chen, Kevin; Pachter, Lior
- PLoS Computational Biology, Vol. 1, Issue 2
Evolution of the RNA Polymerase B' Subunit Gene (rpoB') in Halobacteriales: a Complementary Molecular Marker to the SSU rRNA Gene
journal, August 2004
- Walsh, D. A.
- Molecular Biology and Evolution, Vol. 21, Issue 12
EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data
journal, May 2011
- Miller, Christopher S.; Baker, Brett J.; Thomas, Brian C.
- Genome Biology, Vol. 12, Issue 5
The Earth Microbiome project: successes and aspirations
journal, August 2014
- Gilbert, Jack A.; Jansson, Janet K.; Knight, Rob
- BMC Biology, Vol. 12, Issue 1
Accurate and fast estimation of taxonomic profiles from metagenomic shotgun sequences
journal, January 2011
- Liu, Bo; Gibbons, Theodore; Ghodsi, Mohammad
- BMC Genomics, Vol. 12, Issue Suppl 2
Differentiation of Lactobacillus plantarum, L. pentosus, and L. paraplantarum by recA Gene Sequence Analysis and Multiplex PCR Assay with recA Gene-Derived Primers
journal, August 2001
- Torriani, S.; Felis, G. E.; Dellaglio, F.
- Applied and Environmental Microbiology, Vol. 67, Issue 8
Genomic variation landscape of the human gut microbiome
journal, December 2012
- Schloissnig, Siegfried; Arumugam, Manimozhiyan; Sunagawa, Shinichi
- Nature, Vol. 493, Issue 7430
Metagenomics Using Next-Generation Sequencing
book, January 2014
- Bragg, Lauren; Tyson, Gene W.
- Methods in Molecular Biology
Photosynthetic and Phylogenetic Primers for Detection of Anoxygenic Phototrophs in Natural Environments
journal, July 2001
- Achenbach, L. A.; Carey, J.; Madigan, M. T.
- Applied and Environmental Microbiology, Vol. 67, Issue 7
Use of 16S rRNA and rpoB Genes as Molecular Markers for Microbial Ecology Studies
journal, October 2006
- Case, R. J.; Boucher, Y.; Dahllof, I.
- Applied and Environmental Microbiology, Vol. 73, Issue 1
Toward an Efficient Method of Identifying Core Genes for Evolutionary and Functional Microbial Phylogenies
journal, September 2011
- Segata, Nicola; Huttenhower, Curtis
- PLoS ONE, Vol. 6, Issue 9
A core gut microbiome in obese and lean twins
journal, November 2008
- Turnbaugh, Peter J.; Hamady, Micah; Yatsunenko, Tanya
- Nature, Vol. 457, Issue 7228
Revisiting bacterial phylogeny: Natural and experimental evidence for horizontal gene transfer of 16S rRNA
journal, January 2013
- Kitahara, Kei; Miyazaki, Kentaro
- Mobile Genetic Elements, Vol. 3, Issue 1
Metagenomics: DNA sequencing of environmental samples
journal, October 2005
- Tringe, Susannah Green; Rubin, Edward M.
- Nature Reviews Genetics, Vol. 6, Issue 11
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012
- Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
- Nucleic Acids Research, Vol. 41, Issue D1
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
journal, January 2009
- Cole, J. R.; Wang, Q.; Cardenas, E.
- Nucleic Acids Research, Vol. 37, Issue Database
PhylOTU: A High-Throughput Procedure Quantifies Microbial Community Diversity and Resolves Novel Taxa from Metagenomic Data
journal, January 2011
- Sharpton, Thomas J.; Riesenfeld, Samantha J.; Kembel, Steven W.
- PLoS Computational Biology, Vol. 7, Issue 1
Towards a Genome-Based Taxonomy for Prokaryotes
journal, September 2005
- Konstantinidis, K. T.; Tiedje, J. M.
- Journal of Bacteriology, Vol. 187, Issue 18
Ribosomal RNA diversity predicts genome diversity in gut bacteria and their relatives
journal, March 2010
- Zaneveld, Jesse R.; Lozupone, Catherine; Gordon, Jeffrey I.
- Nucleic Acids Research, Vol. 38, Issue 12
Metagenomic species profiling using universal phylogenetic marker genes
journal, October 2013
- Sunagawa, Shinichi; Mende, Daniel R.; Zeller, Georg
- Nature Methods, Vol. 10, Issue 12
Saliva microbiomes distinguish caries-active from healthy human populations
journal, June 2011
- Yang, Fang; Zeng, Xiaowei; Ning, Kang
- The ISME Journal, Vol. 6, Issue 1
A meta-analysis of changes in bacterial and archaeal communities with time
journal, April 2013
- Shade, Ashley; Gregory Caporaso, J.; Handelsman, Jo
- The ISME Journal, Vol. 7, Issue 8
A simple, fast, and accurate method of phylogenomic inference
journal, January 2008
- Wu, Martin; Eisen, Jonathan A.
- Genome Biology, Vol. 9, Issue 10
A general method applicable to the search for similarities in the amino acid sequence of two proteins
journal, March 1970
- Needleman, Saul B.; Wunsch, Christian D.
- Journal of Molecular Biology, Vol. 48, Issue 3, p. 443-453
The Chaperonin-60 Universal Target Is a Barcode for Bacteria That Enables De Novo Assembly of Metagenomic Sequence Data
journal, November 2012
- Links, Matthew G.; Dumonceaux, Tim J.; Hemmingsen, Sean M.
- PLoS ONE, Vol. 7, Issue 11
Reduced selection leads to accelerated gene loss in Shigella
journal, January 2007
- Hershberg, Ruth; Tang, Hua; Petrov, Dmitri A.
- Genome Biology, Vol. 8, Issue 8
PhyloSift: phylogenetic analysis of genomes and metagenomes
journal, January 2014
- Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric
- PeerJ, Vol. 2
WGSQuikr: Fast Whole-Genome Shotgun Metagenomic Classification
journal, March 2014
- Koslicki, David; Foucart, Simon; Rosen, Gail
- PLoS ONE, Vol. 9, Issue 3
The COG database: an updated version includes eukaryotes
journal, January 2003
- Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D.
- BMC Bioinformatics, Vol. 4, Article No. 41
Rare Events of Intragenus and Intraspecies Horizontal Transfer of the 16S rRNA Gene
journal, July 2015
- Tian, Ren-Mao; Cai, Lin; Zhang, Wei-Peng
- Genome Biology and Evolution, Vol. 7, Issue 8
16S rRNA Gene Sequencing for Bacterial Identification in the Diagnostic Laboratory: Pluses, Perils, and Pitfalls
journal, July 2007
- Janda, J. M.; Abbott, S. L.
- Journal of Clinical Microbiology, Vol. 45, Issue 9
Metagenomic microbial community profiling using unique clade-specific marker genes
journal, June 2012
- Segata, Nicola; Waldron, Levi; Ballarini, Annalisa
- Nature Methods, Vol. 9, Issue 8
Gene sequences useful for predicting relatedness of whole genomes in bacteria
journal, November 2003
- Zeigler, D. R.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 6
Human gut microbes associated with obesity
journal, December 2006
- Ley, Ruth E.; Turnbaugh, Peter J.; Klein, Samuel
- Nature, Vol. 444, Issue 7122
PhyloSift: Phylogenetic analysis of genomes and metagenomes
dataset, January 2013
- Bik, Holly; Matsen, Erick; Lowe, Eric
- Figshare
Using QIIME to Analyze 16S rRNA Gene Sequences from Microbial Communities
journal, December 2011
- Kuczynski, Justin; Stombaugh, Jesse; Walters, William Anton
- Current Protocols in Bioinformatics, Vol. 36, Issue 1
Accurate and fast estimation of taxonomic profiles from metagenomic shotgun sequences
journal, September 2011
- Liu, Bo; Gibbons, Theodore; Ghodsi, Mohammad
- Genome Biology, Vol. 12, Issue S1
Works referencing / citing this record:
Evaluation of the infB and rpsB gene fragments as genetic markers intended for identification and phylogenetic analysis of particular representatives of the order Lactobacillales
journal, July 2018
- Mekadim, C.; Killer, J.; Mrázek, J.
- Archives of Microbiology, Vol. 200, Issue 10
Rapid Genetic Adaptation during the First Four Months of Survival under Resource Exhaustion
journal, March 2017
- Avrani, Sarit; Bolotin, Evgeni; Katz, Sophia
- Molecular Biology and Evolution, Vol. 34, Issue 7
Iroki: automatic customization and visualization of phylogenetic trees
journal, September 2019
- Moore, Ryan M.; Harrison, Amelia O.; McAllister, Sean M.
- PeerJ
Understanding and overcoming the pitfalls and biases of next-generation sequencing (NGS) methods for use in the routine clinical microbiological diagnostic laboratory
journal, March 2019
- Boers, Stefan A.; Jansen, Ruud; Hays, John P.
- European Journal of Clinical Microbiology & Infectious Diseases, Vol. 38, Issue 6
Glutamine synthetase type I (glnAI) represents a rewarding molecular marker in the classification of bifidobacteria and related genera
journal, May 2019
- Killer, Jiří; Mekadim, Chahrazed; Bunešová, Věra
- Folia Microbiologica, Vol. 65, Issue 1
Unveiling Plant-Beneficial Function as Seen in Bacteria Genes from Termite Mound Soil
journal, January 2020
- Enagbonma, Ben Jesuorsemwen; Babalola, Olubukola Oluranti
- Journal of Soil Science and Plant Nutrition, Vol. 20, Issue 2
The vaginal microbiome of pregnant women is less rich and diverse, with lower prevalence of Mollicutes, compared to non-pregnant women
journal, August 2017
- Freitas, Aline C.; Chaban, Bonnie; Bocking, Alan
- Scientific Reports, Vol. 7, Issue 1
A comparative assessment of conventional and molecular methods, including MinION nanopore sequencing, for surveying water quality
journal, October 2019
- Acharya, Kishor; Khanal, Santosh; Pantha, Kalyan
- Scientific Reports, Vol. 9, Issue 1
Generating amplicon reads for microbial community assessment with next‐generation sequencing
journal, August 2019
- Gołębiewski, M.; Tretyn, A.
- Journal of Applied Microbiology, Vol. 128, Issue 2
Comprehensive benchmarking and ensemble approaches for metagenomic classifiers
journal, September 2017
- McIntyre, Alexa B. R.; Ounit, Rachid; Afshinnekoo, Ebrahim
- Genome Biology, Vol. 18, Issue 1
Absolute quantitation of microbiota abundance in environmental samples
journal, June 2018
- Tkacz, Andrzej; Hortala, Marion; Poole, Philip S.
- Microbiome, Vol. 6, Issue 1
A Literature Review of Metagenomics and Culturomics of the Peri-implant Microbiome: Current Evidence and Future Perspectives
journal, September 2019
- Martellacci, Leonardo; Quaranta, Gianluca; Patini, Romeo
- Materials, Vol. 12, Issue 18
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