Evolution of gene order conservation in prokaryotes
Open accessAbstract
BACKGROUND: As more complete genomes are sequenced, conservation of gene order between different organisms is emerging as an informative property of the genomes. Conservation of gene order has been used for predicting function and functional interactions of proteins, as well as for studying the evolutionary relationships between genomes. The reasons for the maintenance of gene order are still not well understood, as the organization of the prokaryote genome into operons and lateral gene transfer cannot possibly account for all the instances of conservation found. Comprehensive studies of gene order are one way of elucidating the nature of these maintaining forces. RESULTS: Gene order is extensively conserved between closely related species, but rapidly becomes less conserved among more distantly related organisms, probably in a cooperative fashion. This trend could be universal in prokaryotic genomes, as archaeal genomes are likely to behave similarly to bacterial genomes. Gene order conservation could therefore be used as a valid phylogenetic measure to study relationships between species. Even between very distant species, remnants of gene order conservation exist in the form of highly conserved clusters of genes. This suggests the existence of selective processes that maintain the organization of these regions. Because the clusters often span more than one operon, common regulation probably cannot be invoked as the cause of the maintenance of gene order. CONCLUSIONS: Gene order conservation is a genomic measure that can be useful for studying relationships between prokaryotes and the evolutionary forces shaping their genomes. Gene organization is extensively conserved in some genomic regions, and further studies are needed to elucidate the reason for this conservation.
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Genome architecture/gene locality is often significantly conserved in related organisms.
“In conjunction with this, biological insight into genome locality (i.e., operonal or transcription unit structure) of related bacterial organisms can assist in clarifying the function of unknown JCVI-syn3A genes since genome architecture/gene locality is often significantly conserved in related organisms.47,48”
From Toward the Complete Functional Characterization of a Minimal Bacterial Proteome (2022) · cites this paper as [47]
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The Incompatible Desiderata of Gene Cluster Properties
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“In this paper we primarily focus on r -windows and max-gap clusters, two cluster definitions that are used in practice [6,7,15,16,17,9,10], but briefly describe other definitions as well.”
BackgroundMethodCruz-Ramos, H., Cook, G., Wu, G.-H., Cleeter, M., & Poole, R. (2004) · Microbiology · doi:10.1099/mic.0.27191-0 · Cited by 47 · see citing works
“The conservation of gene order is obvious between closely related species, but rapidly becomes less conspicuous among more distantly related organisms (Tamames, 2001).”
Evolutionary patterns in prokaryotic genomes.
Rocha, E. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.09.007 · Cited by 43 · see citing works
“The relative order of core genes between pairs of genomes drops exponentially with divergence time [31,32], but is different for certain genomic regions, for example, slower in operons, and depends on the genome relative stability [33 ].”
BackgroundLo, K.-J., Lin, S.-S., Lu, C.-W., Kuo, C.-H., & Liu, C.-T. (2018) · Scientific Reports · doi:10.1038/s41598-018-31128-8 · Cited by 42 · see citing works
Uncovering major genomic features of essential genes in Bacteria and a methanogenic Archaea
Grazziotin, A. L., Vidal, N. M., & Venancio, T. M. (2015) · The FEBS Journal · doi:10.1111/febs.13350 · Cited by 42 · see citing works
Guerrero, G., Peralta, H., Aguilar, A., Díaz, R., Villalobos, M., Medrano-Soto, A., & Mora, J. (2005) · BMC Evolutionary Biology · doi:10.1186/1471-2148-5-55 · Cited by 40
“It was suggested that physiologically important gene clusters could be positively selected, and synteny perhaps reveals the functional constraints of these genes [6].”
BackgroundA Unified Approach for Reconstructing Ancient Gene Clusters
Stoye, J., & Wittler, R. (2009) · IEEE/ACM Transactions on Computational Biology & Bioinformatics · doi:10.1109/tcbb.2008.135 · Cited by 37
“Ç 1INTRODUCTION T HE exploration of phylogenetic relationships of several regions might also provide insight into the evolutionary species yields broad information about their evolution. history of genes.”
Genomic organization of evolutionarily correlated genes in bacteria: limits and strategies.
Junier, I., Hérisson, J., & Képès, F. (2012) · Journal of Molecular Biology · doi:10.1016/j.jmb.2012.03.009 · Cited by 36 · see citing works
Understanding serine proteases implications on Leishmania spp lifecycle.
Alves, C., Souza, R., Charret, K. S., Côrtes, L. M. D. C., de Sá-Silva, M. P., Barral-Veloso, L., de Oliveira, L. F. G., & da Silva, F. S. (2017) · Experimental parasitology · doi:10.1016/j.exppara.2017.11.008 · Cited by 35 · see citing works
“Synten , or conservation of chromosomal 628 gene order, has been proposed as result of the interdep ndence between a gene product and 629 its genomic context (Korbel et al., 2004; Tamames, 2001), including the chromosome and 630 gene copy number variation (Rogers et al., 2011).”
BackgroundAssessment of de novo assemblers for draft genomes: a case study with fungal genomes
Abbas, M., Malluhi, Q., & Balakrishnan, P. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-s9-s10 · Cited by 35 · see citing works
“We can select suitable conservation elements based on the type of organism by hinging on available literature such as [29-33].”
MethodPSAT: A web tool to compare genomic neighborhoods of multiple prokaryotic genomes
Fong, C., Rohmer, L., Radey, M., Wasnick, M., & Brittnacher, M. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-170 · Cited by 35 · see citing works
“Gene order analyses on a local genomic neighborhood level, however, can also be very useful for helping to predict gene function, identify proteins that potentially interact physically, or infer evolutionary relationships between genomes [4,5].”
BackgroundThe Statistical Analysis of Spatially Clustered Genes under the Maximum Gap Criterion
Hoberman, R., Sankoff, D., & Durand, D. (2005) · J. Comput. Biol. · doi:10.1089/cmb.2005.12.1083 · Cited by 35 · see citing works
“1083 Overbeek et al., 1999; Simillion et al., 2002; Tamames, 2001; Vandepoele et al., 2002 Vision et al., 2000).”
BackgroundInfluentialEmergent gene order in a model of modular polyketide synthases
Callahan, B., Thattai, M., & Shraiman, B. (2009) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0902364106 · Cited by 34
“Typically gene order is considered selection-neutral, with degree of conservation even used to estimate phylogenetic distance (17).”
Gene teams with relaxed proximity constraint
Kim, S., Choi, J.-H., & Yang, J. (2005) · IEEE Computer Society Computational Systems Bioinformatics Conference · doi:10.1109/csb.2005.33 · Cited by 32
“We also compared gene clusters from our algorithm with gene order conservation study in [19].”
ResultInfluentialBratlie, M. S., Johansen, J., & Drabløs, F. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-71 · Cited by 31 · see citing works
“Conservation of gene order has been studied in a number of earlier reports [65-67].”
Conserved distances between vertebrate highly conserved elements.
Sun, H., Skogerbø, G., & Chen, R.-S. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl232 · Cited by 31 · see citing works
“The measure of UCE or gene order conservation between two genomes used here is the ratio between the number of UCEs or genes linked in conserved runs and the total number of related UCEs or genes ( 26 ).”
BackgroundResultInfluentialZaneveld, J. R., & Thurber, R. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00431 · Cited by 29 · see citing works
“The strongest single factor limiting the accuracy of predictions made by HSP is the availability of phylogenetically diverse reference data.”
BackgroundMuley, V., & Ranjan, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042057 · Cited by 29 · see citing works
“The better performance of GAMMA could be explained by the fact that the gene order, gene content and regulatory mechanisms of operons are not conserved even in closely related species [23,24,32,59].”
BackgroundMahadevan, P., King, J. F., & Seto, D. (2009) · Int. J. Comput. Biol. Drug Des. · doi:10.1504/ijcbdd.2009.027586 · Cited by 29
“The analysis of gene order, and the conservation of gene order (synteny), is important for understanding the evolution of genomes and the evolutionary relationships between them (Tamames, 2001).”
BackgroundComparative genomics and functional annotation of bacterial transporters
Gelfand, M., & Rodionov, D. (2008) · Physics of Life Reviews · doi:10.1016/j.plrev.2007.10.003 · Cited by 29 · see citing works
“An indirect way to assign a cellular role to an uncharacterized gene is to take into account its chromosomal localization [31,53,82,151,229,260]; reviewed in [142,148,153,203].”
BackgroundLin, C.-H., Bourque, G., & Tan, P. (2008) · Molecular biology and evolution · doi:10.1093/molbev/msm282 · Cited by 29 · see citing works
“We hypothesized that if the cellular functions mediated by these clusters are important units that are conserved and required through evolution, genes in these units should thus be preferentially be preserved within synteny blocks (Tamames 2001).”
Comparing bacterial genomes through conservation profiles.Preprint
Martin, M., Herrero, J., Mateos, Á., & Dopazo, J. (2003) · Genome Research · doi:10.1101/gr.678303 · Cited by 29 · see citing works
“…order is extensively conserved between closely related bacterial species, and archaeal genomes are likely to behave similarly to bacterial genomes (Tamames 2001) Even across very distant species, remnants of gene order conservation exist in the form of highly conserved clusters of genes This…”
BackgroundLagomarsino, M., Espéli, O., & Junier, I. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.07.002 · Cited by 26 · see citing works
Toward the Complete Functional Characterization of a Minimal Bacterial Proteome
Bianchi, D. M., Pelletier, J. F., Hutchison, C. A., Glass, J. I., & Luthey-Schulten, Z. (2022) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.2c04188 · Cited by 22 · see citing works
Architecture and genomic arrangement of the MurE–MurF bacterial cell wall biosynthesis complex
Shirakawa, K. T., Sala, F. A., Miyachiro, M. M., Job, V., Trindade, D., & Dessen, A. (2023) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2219540120 · Cited by 25 · see citing works
“In some species and during specific growth phases, several genes in the cluster are co-transcribed as long polycistronic RNAs, originating from promoters located upstream from murE (26, 28) (Fig.”
BackgroundMitochondrial Genome Evolution in Pelagophyte Algae
Sibbald, S. J., Lawton, M., & Archibald, J. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab018 · Cited by 24 · see citing works
“All things considered, it seems likely that the hypothetical ribosomal proteins in A. lagunensis are orthologous but divergent versions of the known ribosomal proteins in related pelagophytes (Huynen et al. 2000; Tamames 2001).”
BackgroundGene Cluster Statistics with Gene Families
Raghupathy, N., & Durand, D. (2009) · Molecular biology and evolution · doi:10.1093/molbev/msp002 · Cited by 24
“…gene order, and identification of horizontal gene transfer events (Dandekar et al. 1998; Huynen and Bork 1998; Overbeek et al. 1999; Tamames 2001; Tamames et al. 2001; Zheng et al. 2002; Chen et al. 2004; Hurst et al. 2004; Bourque et al. 2005; Murphy et al. 2005; Homma et al. 2007; von Mering…”
BackgroundYan, Y., & Moult, J. (2006) · Proteins: Structure, Function, and Bioinformatics · doi:10.1002/prot.21021 · Cited by 22
“Overbeek et al. 11,14,15 developed a method that estimates the likelihood that a conserved gene pair could be in an operon, and benchmarked the result with the RegulonDB data set.”
ResultPositional Homology in Bacterial Genomes
Burgetz, I., Shariff, S., Pang, A., & Tillier, E. (2006) · Evolutionary bioinformatics online · doi:10.1177/117693430600200031 · Cited by 22
“…beyond the genus level, there is still considerable gene order conservation between many of the available sequenced bacterial genomes (Huynen and Bork 1998, Tamames 2001, Tillier and Collins 2000, Wong and Golding 2003; also see examples at http://www.uhnres.utoronto.ca/ tillier/Xplots.html).”
BackgroundThe origin and evolution of eucaryal HIS7 genes: from metabolon to bifunctional proteins?
Brilli, M., & Fani, R. (2004) · Gene · doi:10.1016/j.gene.2004.06.033 · Cited by 22 · see citing works
Pust, M.-M., & Tümmler, B. (2021) · ISME Communications · doi:10.1038/s43705-021-00010-6 · Cited by 21 · see citing works
Conserved patterns in bacterial genomes: A conundrum physically tailored by evolutionary tinkering
Junier, I. (2014) · Comput. Biol. Chem. · doi:10.1016/j.compbiolchem.2014.08.017 · Cited by 21 · see citing works
“…rearrangement, gene loss, and ene transpositions, including horizontal transfer), the conservaion of gene clusters extends beyond the scale of operons (Lathe t al., 2000; Tamames, 2001; Audit and Ouzounis, 2003; Rocha, 006; Fang et al., 2008; Junier et al., 2012; Junier and Rivoire, 013).”
BackgroundJaruszewicz, J., Kimmel, M., & Lipniacki, T. (2014) · Physical review. E, Statistical, nonlinear, and soft matter physics · doi:10.1103/physreve.89.022710 · Cited by 21 · see citing works
Brandis, G., & Hughes, D. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008615 · Cited by 19 · see citing works
“A remarkable example of conservation of an ancient co-linear organization of gene is found for a large set of genes involved in transcription and translation [8].”
BackgroundLi, J., Halgamuge, S., Kells, C., & Tang, S.-L. (2007) · BMC Bioinformatics · doi:10.1186/1471-2105-8-s4-s6 · Cited by 19
“genomic context information such as co-occurrence of genes [6,7] and conservation of gene order [8,9].”
BackgroundThe Statistical Significance of Max-Gap Clusters
Hoberman, R., Sankoff, D., & Durand, D. (2004) · Comparative Genomics · doi:10.1007/978-3-540-32290-0_5 · Cited by 19
“The most stringent of these define conserved segments as two or more contiguous regions that contain the same genes in the same order [42, 44] and sometimes orientation [45, 60, 68].”
BackgroundMethodInfluentialMuGeN: Simultaneous Exploration of Multiple Genomes and Computer Analysis Results
Hoebeke, M., Nicolas, P., & Bessières, P. (2003) · Bioinform. · doi:10.1093/bioinformatics/btg101 · Cited by 19
Large-scale analysis of gene clustering in bacteria.
Yang, Q., & Sze, S.-H. (2008) · Genome Research · doi:10.1101/gr.072322.107 · Cited by 18
“In addition to common gene orientations, the spatial arrangement of genes within bacterial operons is important for function, expression, and regulation of these genes (Itoh et al. 1999; Tamames 2001).”
BackgroundToo Much of a Good Thing: How Ectopic DNA Replication Affects Bacterial Replication Dynamics
Syeda, A., Dimude, J. U., Skovgaard, O., & Rudolph, C. J. (2020) · Frontiers in Microbiology · doi:10.3389/fmicb.2020.00534 · Cited by 17 · see citing works
“In addition, global gene order is surprisingly conserved between closely related prokaryotic species (Tamames, 2001).”
BackgroundWeber, L., Thoelken, C., Volk, M., Remes, B., Lechner, M., & Klug, G. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165694 · Cited by 17
Metagenomic Guilt by Association: An Operonic Perspective
Vey, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071484 · Cited by 17 · see citing works
“gene order) is only weakly conserved across bacterial and archaeal genomes [17,18].”
BackgroundDoes Gene Translocation Accelerate the Evolution of Laterally Transferred Genes?
Hao, W.-L., & Golding, G. B. (2009) · Genetics · doi:10.1534/genetics.109.104216 · Cited by 17 · see citing works
G-NEST: a gene neighborhood scoring tool to identify co-conserved, co-expressed genes
Lemay, D. G., Martin, W. F., Hinrichs, A. S., Rijnkels, M., German, J. B., Korf, I. F., & Pollard, K. S. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-253 · Cited by 18 · see citing works
“While ortholog mapping has been used successfully to determine neighborhood conservation in prokaryotes [36,37,41-46], it is less appropriate for mammalian genomes because the maps are incomplete, resulting in many neighborhoods being falsely identified as non-conserved.”
BackgroundResultThe pseudogenes of Mycobacterium leprae reveal the functional relevance of gene order within operons
Muro, E. M., Mah, N., Moreno-Hagelsieb, G., & Andrade, M. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1067 · Cited by 16 · see citing works
Elevated Rate of Genome Rearrangements in Radiation-Resistant Bacteria
Repar, J., Supek, F., Klanjšček, T., Warnecke, T., Zahradka, K., & Zahradka, D. (2017) · Genetics · doi:10.1534/genetics.116.196154 · Cited by 15 · see citing works
“Genome-rearrangement distances between species pairs in each data set were estimated using the differences in the ordering of orthologs between genomes, a commonly used approach (e.g., Suyama and Bork 2001; Tamames 2001; Belda et al. 2005; Rocha 2006; Aguileta et al. 2014).”
MethodRapid pair-wise synteny analysis of large bacterial genomes using web-based GeneOrder4.0
Mahadevan, P., & Seto, D. (2010) · BMC Research Notes · doi:10.1186/1756-0500-3-41 · Cited by 15
“Software tools have been developed for the analysis of gene order and synteny, which are important because they can be used to understand prokaryotic relationships and the evolution of their genomes [2], as well as to aid in gene function annotation [3], and to parse functional coupling prediction between genes in gen…”
Method
- Authors
- Tamames, J.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Corresponding author
- Tamames, Javier
- ORCID
- Tamames, Javier
- Venue
- Genome Biology
- Published
- 2001-06-01
- Volume
- 2
- Issue
- 6
- Pages
- RESEARCH0020-RESEARCH0020
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC33396
- OpenAlex
- W1598176384
- Cited by
- 213
- References
- 29
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 3 · 2023: 3 · 2022: 5 · 2021: 5 · 2020: 8 · 2019: 4 · 2018: 4 · 2017: 5 · 2016: 8 · 2015: 3 · 2014: 12 · 2013: 12 · 2012: 8
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Genome biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, other-oa)
- Funders
- Centro Nacional de Biotecnología
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- gene order conservation, prokaryotic genomes, genome organization, gene clusters, operon, horizontal gene transfer, archaeal genomes, genome evolution, gene expression regulation
- MeSH terms
- Phylogeny, Genome, Bacterial, Conserved Sequence, Evolution, Molecular, Genome, Archaeal, Gene Order
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