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Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes
Open accessAbstract
Gene duplication followed by neo- or sub-functionalization deeply impacts the evolution of protein families and is regarded as the main source of adaptive functional novelty in eukaryotes. While there is ample evidence of adaptive gene duplication in prokaryotes, it is not clear whether duplication outweighs the contribution of horizontal gene transfer in the expansion of protein families. We analyzed closely related prokaryote strains or species with small genomes (Helicobacter, Neisseria, Streptococcus, Sulfolobus), average-sized genomes (Bacillus, Enterobacteriaceae), and large genomes (Pseudomonas, Bradyrhizobiaceae) to untangle the effects of duplication and horizontal transfer. After removing the effects of transposable elements and phages, we show that the vast majority of expansions of protein families are due to transfer, even among large genomes. Transferred genes--xenologs--persist longer in prokaryotic lineages possibly due to a higher/longer adaptive role. On the other hand, duplicated genes--paralogs--are expressed more, and, when persistent, they evolve slower. This suggests that gene transfer and gene duplication have very different roles in shaping the evolution of biological systems: transfer allows the acquisition of new functions and duplication leads to higher gene dosage. Accordingly, we show that paralogs share most protein-protein interactions and genetic regulators, whereas xenologs share very few of them. Prokaryotes invented most of life's biochemical diversity. Therefore, the study of the evolution of biology systems should explicitly account for the predominant role of horizontal gene transfer in the diversification of protein families.
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“Recent theoretical, comparative genomic and experimental research on microbial evolution clearly indicates that HGT is the principal factor in microbial adaptation and innovation (46, 65, 66, 80).”
From Origin and Evolution of the Universal Genetic Code (2017) · cites this paper as [80]
Experimental — accuracy not yet measuredIn the citing paper
“Given that HGT, even if limited by both physical and selective barriers, remained a key factor of microbial evolution [36,37,38,39,40], and apparently, a condition for long term survival of microbial populations [41,42]”
From Frozen Accident Pushing 50: Stereochemistry, Expansion, and Chance in the Evolution of the Genetic Code (2017) · cites this paper as [40]
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ICEscreen: a tool to detect Firmicute ICEs and IMEs, isolated or enclosed in composite structures
Lao, J., Lacroix, T., Guédon, G., Coluzzi, C., Payot, S., Leblond‐Bourget, N., & Chiapello, H. (2022) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqac079 · Cited by 34
“Horizontal gene transfer constitutes a major evolutionary force among bacterial genomes (1,2).”
BackgroundMolecular Phylogenetics and the Perennial Problem of Homology
Inkpen, S. A., & Doolittle, W. F. (2016) · Journal of Molecular Evolution · doi:10.1007/s00239-016-9766-4 · Cited by 34
Locating a Tree in a Phylogenetic Network in Quadratic Time
Gambette, P., Gunawan, A. D. M., Labarre, A., Vialette, S., & Zhang, L. (2015) · Lecture notes in computer science · doi:10.1007/978-3-319-16706-0_12 · Cited by 33
Bhandari, V., Naushad, H. S., & Gupta, R. S. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00098 · Cited by 35
“…| Volume 2 | Article 98 | 1 CELLULAR AND INFECTION MICROBIOLOGY evolution of new genes by gene duplication and divergence, gain of new genes by means of LGTs, as well as gene losses in various lineages (Bapteste et al., 2009; Ragan and Beiko, 2009; Treangen and Rocha, 2011; Williams et al., 2011).”
BackgroundKoumandou, V. L., & Κοσσίδα, Σ. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003821 · Cited by 34
“Given the widespread effect of HGT on prokaryotic evolution [38,39,40], it may be that the cost of incorporating a laterally transferred ATP synthase to replace a pre-existing enzyme is too high to overcome [41].”
BackgroundUnleashing Natural Competence in Lactococcus lactis by Induction of the Competence Regulator ComX
Mulder, J., Wels, M., Kuipers, O. P., Kleerebezem, M., & Bron, P. A. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.01320-17 · Cited by 34
“Horizontal gene transfer (HGT) fulfills an important role in the evolution of bacteria (1-4).”
BackgroundPromoter propagation in prokaryotes
Matus, M. G., Nijveen, H., & van Passel, M. W. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks787 · Cited by 33
Zhang, X., Liu, X., He, Q., Dong, W., Zhang, X., Fan, F., Peng, D., Huang, W., & Yin, H. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01960 · Cited by 31
“…of horizontal (lateral) gene transfer (HGT) in the expansion of gene repertoires of prokaryotes (Ochman et al., 2000; Gogarten et al., 2002; Treangen and Rocha, 2011), we inferred that the frequency of HGT was high in group 2 strains with larger genomes, conferring a predominant role in…”
BackgroundHorizontal gene transfer in an acid mine drainage microbial community
Guo, J., Wang, Q., Wang, X., Wang, F., Yao, J., & Zhu, H. (2015) · BMC Genomics · doi:10.1186/s12864-015-1720-0 · Cited by 31
“Many viewpoints, which were formed by studying individual prokaryotic genomes, suggested that HGT events contributed to the evolution and adaptation of species [18].”
BackgroundGenome Rearrangements Can Make and Break Small RNA Genes
Raghavan, R., Kacharia, F. R., Millar, J. A., Sislak, C. D., & Ochman, H. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv009 · Cited by 32
“The source of this variation has been ascribed not only to the differences among species in their repertoires of DNA recombination and repair enzymes (Tamas et al. 2002) but also to selection on gene order and position (Suyama and Bork 2001; Ballouz et al. 2010; Treangen and Rocha 2011).”
BackgroundFrom proteins to polysaccharides: lifestyle and genetic evolution of Coprothermobacter proteolyticus
Kunath, B. J., Delogu, F., Naas, A. E., Arntzen, M. Ø., Eijsink, V. G. H., Henrissat, B., Hvidsten, T. R., & Pope, P. B. (2018) · The ISME Journal · doi:10.1038/s41396-018-0290-y · Cited by 32
Insights into early evolutionary adaptations of the Akkermansia genus to the vertebrate gut
González, D., Morales-Olavarria, M., Vidal-Veuthey, B., & Cárdenas, J. P. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1238580 · Cited by 30
“Likewise, it has been shown that the adaptation of bacteria to new environments is mainly mediated by the expansion of protein families encoded by genes obtained through HGT and not by gene duplication (Treangen and Rocha, 2011).”
BackgroundA decomposition theorem and two algorithms for reticulation-visible networks
Gunawan, A. D. M., DasGupta, B., & Zhang, L. (2016) · Information and Computation · doi:10.1016/j.ic.2016.11.001 · Cited by 30
“have demonstrated that genetic material is often transfered between organisms in a nonreproductive manner [4, 25], it has been commonly accepted that phylogenetic networks are more suitable than phylogenetic trees for modeling reticulation events such as horizontal”
BackgroundPathogenomics insights for understanding Pasteurella multocida adaptation
Raquel Hurtado, C., Lenin Maturrano, H., Azevedo, V., & Aburjaile, F. F. (2020) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2020.151417 · Cited by 33
Castro‐Fernández, V., Herrera-Morandé, A., Zamora, R. A., Merino, F., Gonzalez-Ordenes, F., Padilla-Salinas, F., Pereira, H. M., Brandão-Neto, J., Garratt, R. C., & Guixé, V. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.790865 · Cited by 27
“Furthermore, evidence shows the importance and high rate of HGT events occurring during the evolution of prokaryotes in general (29).”
BackgroundCoevolving Plasmids Drive Gene Flow and Genome Plasticity in Host-Associated Intracellular Bacteria
Köstlbacher, S., Collingro, A., Halter, T., Domman, D., & Horn, M. (2020) · Current Biology · doi:10.1016/j.cub.2020.10.030 · Cited by 29
“HGT is a major driver of microbial genome evolution, promoting the adaptation to novel environmental conditions.(78) It is considered particularly important for strictly intracellular bacteria as it provides another means to escape Muller’s ratchet.”
A two‐step evolutionary process establishes a non‐native vitamin B6 pathway in Bacillus subtilis
Rosenberg, J., Yeak, K. Y. C., & Commichau, F. M. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13950 · Cited by 30
Building a better bacillus: the emergence of Mycobacterium tuberculosis
Wang, J., & Behr, M. A. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00139 · Cited by 29
“MINI REVIEW ARTICLE published: 03 April 2014 doi: 10.3389/fmicb.2014.00139 Building a better bacillus: the emergence of Mycobacterium tuberculosis”
BackgroundMethodInfluentialGarcia‐Garcerà, M., Touchon, M., Brisse, S., & Rocha, E. P. C. (2017) · Environmental Microbiology · doi:10.1111/1462-2920.13949 · Cited by 31
“The evolution of many bacterial lineages, like Acinetobacter, is driven by rapid change in gene repertoires in response to environmental challenges (Ley et al., 2006; Treangen and Rocha, 2011).”
BackgroundSelf-citationVallino, J. J., & Huber, J. A. (2018) · Frontiers in Environmental Science · doi:10.3389/fenvs.2018.00100 · Cited by 25
Systematic Detection of Large-Scale Multigene Horizontal Transfer in Prokaryotes
Kloub, L. H., Gosselin, S. P., Fullmer, M. S., Graf, J., Gogarten, J. P., & Bansal, M. S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab043 · Cited by 27
Pan-Genome-Wide Analysis of Pantoea ananatis Identified Genes Linked to Pathogenicity in Onion
Agarwal, G., Choudhary, D., Stice, S. P., Myers, B. K., Gitaitis, R. D., Venter, S. N., Kvitko, B. H., & Dutta, B. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.684756 · Cited by 28
The Role of Reticulate Evolution in Creating Innovation and Complexity
Swithers, K. S., Soucy, S. M., & Gogarten, J. P. (2012) · International Journal of Evolutionary Biology · doi:10.1155/2012/418964 · Cited by 33
“In Bacteria and Archaea autochthonous gene duplications appear to be rare [42, 96].”
BackgroundEvolution of substrate specificity in a retained enzyme driven by gene loss
Juárez-Vázquez, A. L., Edirisinghe, J. N., Verduzco-Castro, E. A., Michalska, K., Wu, C., Noda‐García, L., Babnigg, G., Endres, M. J., Medina-Ruiz, S., Santoyo-Flores, J., et al. (2017) · eLife · doi:10.7554/elife.22679 · Cited by 29
Horizontally Acquired Biosynthesis Genes Boost Coxiella burnetii's Physiology
Moses, A. S., Millar, J. A., Bonazzi, M., Beare, P. A., & Raghavan, R. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00174 · Cited by 30
“burnetii HGT is a major driver of evolution and adaptation in bacteria (Lerat et al., 2005; Price et al., 2008; Treangen and Rocha, 2011).”
BackgroundMancini, J., Weckselblatt, B., Chung, Y. K., Durante, J. C., Andelman, S. M., Glaubman, J., Dorff, J. D., Bhargava, S., Lijek, R. S., Unger, K. P., et al. (2011) · Journal of Bacteriology · doi:10.1128/jb.05142-11 · Cited by 28
“Additionally, horizontal transfer into organisms that have adapted differently to host selection may account for evolution of different functions among members of very similar gene families, an example of how horizontal gene transfer can shape protein family expansion (41).”
BackgroundNatural Selection for Operons Depends on Genome Size
Nuñez, P. A., Romero, H., Farber, M. D., & Rocha, E. P. C. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt174 · Cited by 30
“Key words: operons, prokaryotes, evolution.”
BackgroundSelf-citationAres-Arroyo, M., Rocha, E. P. C., & González‐Zorn, B. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009919 · Cited by 27
“They play a crucial role in bacterial evolution as they are key drivers of horizontal gene transfer, the major process of gene repertoire variation in prokaryotes [2].”
BackgroundSelf-citationModular evolution of secretion systems and virulence plasmids in a bacterial species complex
Chou, L., Lin, Y.-C., Haryono, M., Santos, M. N. M., Cho, S., Weisberg, A. J., Wu, C., Chang, J. H., Lai, E., & Kuo, C. (2022) · BMC Biology · doi:10.1186/s12915-021-01221-y · Cited by 27
“to the hypothesis that HGT is more important than duplications in driving gene family expansions in bacteria [79].”
BackgroundDowning, T. (2015) · Microorganisms · doi:10.3390/microorganisms3020236 · Cited by 26
“Genes arising by HGT are frequently associated with duplications, which can permit new functions among the two gene copies [99].”
BackgroundA meta-approach for improving the prediction and the functional annotation of ortholog groups
Pereira, C., Denise, A., & Lespinet, O. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-s6-s16 · Cited by 29
“However, this last step becomes an issue when horizontal gene transfer plays a major role in the evolution of the organisms [21].”
BackgroundAn evolutionary analysis of genome expansion and pathogenicity in Escherichia coli
Bohlin, J., Brynildsrud, O. B., Sekse, C., & Snipen, L. G. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-882 · Cited by 27
“Conclusions Our results support previous studies arguing that acquisition of traits through HGT may be a consequence of “spandrel”-like evolutionary processes [33] where the functions of acquired genes are formed through positive selection over time or eventually lost [34,35].”
ResultInterest of bacterial pangenome analyses in clinical microbiology
Anani, H., Zgheib, R., Hasni, I., Raoult, D., & Fournier, P. (2020) · Microbial Pathogenesis · doi:10.1016/j.micpath.2020.104275 · Cited by 28
Joint scaling laws in functional and evolutionary categories in prokaryotic genomes
Grilli, J., Bassetti, B., Maslov, S., & Lagomarsino, M. C. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr711 · Cited by 26
“In reality this move can come either by the virtue of gene duplication or by horizontal gene transfer, which appears to be the dominant class-expansion mechanism in bacteria (9).”
Background
Metadata
- Authors
- Treangen, T. J., & Rocha, E. P. C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Treangen, Todd J.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-01-27
- Volume
- 7
- Issue
- 1
- Pages
- e1001284
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3029252
- OpenAlex
- W2022927779
- Cited by
- 509
- References
- 75
- Citations by year
- 2026: 18 · 2025: 34 · 2024: 36 · 2023: 26 · 2022: 29 · 2021: 32 · 2020: 52 · 2019: 27 · 2018: 33 · 2017: 31 · 2016: 38 · 2015: 29 · 2014: 34 · 2013: 33 · 2012: 28
- FWCI
- 15.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, other-oa)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- horizontal gene transfer, gene duplication, protein family expansion, prokaryotes, paralogs, functional novelty, gene dosage, protein-protein interaction, regulatory genes, genome size, Helicobacter, Neisseria, Streptococcus, Sulfolobus, Bacillus, Enterobacteriaceae, Pseudomonas, Bradyrhizobiaceae
- MeSH terms
- Bacillus, Bacteria, Enterobacteriaceae, Multigene Family, Neisseria, Phylogeny, Pseudomonas, Streptococcus, Genome, Bacterial, Sulfolobus, Helicobacter, Evolution, Molecular, Computational Biology, Gene Duplication, Gene Transfer, Horizontal, Bradyrhizobiaceae
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