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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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“As such, expansions are a particular case of the processes leading to the horizontal transfer of genetic information that is known to shape metabolic [59], genetic [53] and interaction networks [60,61] in prokaryotes.”
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ResultHorizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli
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ResultExtensive repetitive DNA facilitates prokaryotic genome plasticity
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Multiple pathways of selected gene amplification during adaptive mutation
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MethodOrigin and fate of repeats in bacteria
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The impact of long-distance horizontal gene transfer on prokaryotic genome size
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“As a result, PPI networks will evolve very differently in lineages affected by horizontal transfer relative to lineages with strictly vertical transmission of genetic information.”
BackgroundInfluentialDuplication is more common among laterally transferred genes than among indigenous genes
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“coli, where genes with the lowest CAI were found to be overrepresented among recent duplications [30], this discrepancy probably results from our explicit removal of IS and phages that have very low CAI because they are A+T rich and are lowly expressed under exponential growth.”
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“At these distances, gene order conservation is high [58], and positional information can significantly decrease classification errors [72].”
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ResultSelf-citationNew insights into the regulatory networks of paralogous genes in bacteria
Martínez‐Núñez, M. A., Pérez‐Rueda, E., Gutiérrez-Ríos, R.-M., & Merino, E. (2009) · Microbiology · doi:10.1099/mic.0.033266-0 · Cited by 38
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“. Such variations in genome size are typically associated with expansions and contractions of protein families. Expansions of protein families are associated with the acquisition of novel functions, novel regulatory structures and system robustness”
BackgroundOn the need for widespread horizontal gene transfers under genome size constraint
Isambert, H., & Stein, R. R. (2009) · Biology Direct · doi:10.1186/1745-6150-4-28 · Cited by 26 · cited 1×
“It has been proposed that due to deletion biases in prokaryotes, gene duplications are not afforded with sufficient opportunity for neo- or sub-functionalization, reducing its role to transient gene amplification [57].”
BackgroundA Novel Heuristic for Local Multiple Alignment of Interspersed DNA Repeats
Treangen, T. J., Darling, A. E., Achaz, G., Ragan, M. A., Messeguer, X., & Rocha, E. P. C. (2009) · IEEE Transactions on Computational Biology and Bioinformatics · doi:10.1109/tcbb.2009.9 · Cited by 16 · cited 1×
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MethodSelf-citationErosion of interaction networks in reduced and degraded genomes
Ochman, H., Liu, R., & Rocha, E. P. C. (2007) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21147 · Cited by 13 · cited 1×
“As such, expansions are a particular case of the processes leading to the horizontal transfer of genetic information that is known to shape metabolic [59], genetic [53] and interaction networks [60,61] in prokaryotes.”
BackgroundSelf-citation
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- G Vernikos, 2007, Genetic flux over time in the Salmonella lineage., Genome Biology, 8, R100, 10.1186/gb-2007-8-6-r100 · DOI
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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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