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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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“These mobile elements are considered as the most abundant source of HGT in prokaryotes [11–13] and, therefore, they could be key factors to explain the high plasticity and complexity found in GBS genomes.”
Prokaryotic Genome Expansion Is Facilitated by Phages and Plasmids but Impaired by CRISPR
Gao, N., Chen, J., Wang, T., Lercher, M. J., & Chen, W. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02254 · Cited by 13
Distribution of RecBCD and AddAB recombination-associated genes among bacteria in 33 phyla
Gurung, D., & Blumenthal, R. (2020) · Microbiology · doi:10.1099/mic.0.000980 · Cited by 12
Marmon, L. (2013) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2013.07.010 · Cited by 13
Zhu, D., Yang, Z., Xu, J., Wang, M., Jia, R., Chen, S., Liu, M., Zhao, X., Yang, Q., Wu, Y., et al. (2019) · Functional & Integrative Genomics · doi:10.1007/s10142-019-00715-x · Cited by 13
Murawska, E., Fiedoruk, K., & Święcicka, I. (2014) · Polish Journal of Microbiology · doi:10.33073/pjm-2014-020 · Cited by 13
Natural tuning of restriction endonuclease synthesis by cluster of rare arginine codons
Mruk, I., Kaczorowski, T., & Witczak, A. (2019) · Scientific Reports · doi:10.1038/s41598-019-42311-w · Cited by 13
With a Little Help from Prokaryotes
Rocha, E. P. C. (2013) · Science · doi:10.1126/science.1234938 · Cited by 13
Self-citationSIZE DISTRIBUTION OF GENE FAMILIES IN A GENOME
Rudnicki, R., & Tiuryn, J. (2013) · Mathematical Models and Methods in Applied Sciences · doi:10.1142/s0218202513500644 · Cited by 12
Microbial Evolution: Xenology (Apparently) Trumps Paralogy
Eme, L., & Doolittle, W. F. (2016) · Current Biology · doi:10.1016/j.cub.2016.09.049 · Cited by 10
Origin and evolution of gene families in Bacteria and Archaea
Collins, R. E., Merz, H., & Higgs, P. G. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-s9-s14 · Cited by 13
Rocha, E. P. C. (2016) · PLoS Biology · doi:10.1371/journal.pbio.1002417 · Cited by 12
“Horizontal gene transfer (HGT) is a key contributor to the genetic diversification of prokaryotes [1].”
BackgroundSelf-citationLi, S., Qin, K., Li, H., Guo, J., Li, D., Liu, F., Tan, Z., Yan, W., Qu, S., & Zhao, H. (2018) · Electronic Journal of Biotechnology · doi:10.1016/j.ejbt.2018.06.001 · Cited by 12
Fungal Horizontal Gene Transfer: A History Beyond the Phylogenetic Kingdoms
Barreiro, C., Gutiérrez, S., & Olivera, E. R. (2019) · Springer eBooks · doi:10.1007/978-3-030-21862-1_13 · Cited by 13
Parameter Estimation and Species Tree Rooting Using ALE and GeneRax
Williams, T. A., Davín, A., Morel, B., Szánthó, L. L., Spang, A., Stamatakis, A., Hugenholtz, P., & Szöllősi, G. J. (2023) · Genome Biology and Evolution · doi:10.1093/gbe/evad134 · Cited by 12
“Some previous studies (Lerat et al. 2005; Treangen and Rocha 2011; Tria and Martin 2021) have suggested that horizontal gene transfer (HGT) is very common in archaeal and bacterial genomes but less frequent in eukaryotes.”
Lagergård, T., Bölin, I., & Lindholm, L. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06193.x · Cited by 11
Horizontal gene transfers as metagenomic gene duplications
Grassi, L., Caselle, M., Lercher, M. J., & Lagomarsino, M. C. (2012) · Molecular BioSystems · doi:10.1039/c2mb05330f · Cited by 11
Extreme Deviations from Expected Evolutionary Rates in Archaeal Protein Families
Petitjean, C., Makarova, K. S., Wolf, Y. I., & Koonin, E. V. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx189 · Cited by 10
Fei, X., Li, Q., Olsen, J. E., & Jiao, X. (2020) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2020.104446 · Cited by 11
KOMB: K-core based de novo characterization of copy number variation in microbiomes
Balaji, A., Sapoval, N., Seto, C., Elworth, R. A. L., Fu, Y., Nute, M., Savidge, T., Segarra, S., & Treangen, T. J. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.06.019 · Cited by 11
“Communities in metagenomes consist of individual organisms whose genomes are dynamic because of Structural Variants (SVs) such as gene duplication, gene loss/gain, horizontal gene transfer, and gene rearrangements [4–7].”
BackgroundSelf-citationBremer, N., Knopp, M. R., Martin, W. F., & Tria, F. D. K. (2022) · Life · doi:10.3390/life12070995 · Cited by 10
“To see what effect the use of a more realistic T:D ratio would have on the inference of the bacterial root, we set the T:D ratio to values that agree with previous studies [21,22], and repeated the analyses following the same protocol as in Coleman et al.”
BackgroundMethodResultPosadas‐García, Y. S., & Espinosa‐Soto, C. (2022) · BMC Bioinformatics · doi:10.1186/s12859-022-05067-1 · Cited by 10
Enhancing metagenomic classification with compression-based features
Silva, J. M., & Almeida, J. R. (2024) · Artificial Intelligence in Medicine · doi:10.1016/j.artmed.2024.102948 · Cited by 10
Horizontal Acquisition of Prokaryotic Genes for Eukaryote Functioning and Niche Adaptation
Bruto, M., Prigent‐Combaret, C., Luis, P., Hoff, G., Moënne‐Loccoz, Y., & Muller, D. A. E. (2013) · Springer eBooks · doi:10.1007/978-3-642-38212-3_11 · Cited by 10
Large-scale dynamics of horizontal transfers
Grassi, L., Grilli, J., & Lagomarsino, M. C. (2012) · Mobile Genetic Elements · doi:10.4161/mge.21112 · Cited by 9
“However, as we discussed, prokaryotes tend to add genes by HGT rather than by gene duplication.(11,12,14) This behavior also affects the statistics of (domain) functional categories, which in the case of domains are typically made of the sum of a number of evolutionary classes, and empirically grow as power laws(30) w…”
BackgroundSolving the Tree Containment Problem for Genetically Stable Networks in Quadratic Time
Gambette, P., Gunawan, A. D. M., Labarre, A., Vialette, S., & Zhang, L. (2016) · Lecture notes in computer science · doi:10.1007/978-3-319-29516-9_17 · Cited by 10
“in the case of bacterial genomes [9], and many gene families need to be examined.”
BackgroundWillingham-Lane, J. M., Coulson, G. B., & Hondalus, M. K. (2018) · PLoS ONE · doi:10.1371/journal.pone.0204475 · Cited by 10
Li, Z., Pang, B., Wang, D., Li, J., Xu, J., Fang, Y., Lü, X., & Kan, B. (2019) · BMC Genomics · doi:10.1186/s12864-019-5725-y · Cited by 10
Clustering evolving proteins into homologous families
Chan, C. X., Mahbob, M., & Ragan, M. A. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-120 · Cited by 10
“In addition to these three categories, MCL [9], adopting probability and graph flow theory within a Markov matrix framework, has been widely adopted for delineating families in phylogenetic studies [10-14].”
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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