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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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“…in the frequency of substitutions, and thus are within the ideal range for dN/dS analysis (Castillo-Davis et al. 2004; Larracuente et al. 2008; Treangen and Rocha 2011) (for example, from M0 dN/ dS values [that is, the single clade-wide measure of dN/ dS; Stanley and Kulathinal 2016], we…”
Why is Abiogenesis Such a Tough Nut to Crack?
Abel, D. L. (2024) · Archives of Microbiology & Immunology · doi:10.26502/ami.936500182 · Cited by 3
Genomic Rearrangements and Evolution
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Estimation of Gene Insertion/Deletion Rates with Missing Data
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“Lateral gene transfer is an important, yet traditionally underestimated, mechanism for microbial evolution (Treangen and Rocha, 2011; McDaniel et al., 2010).”
BackgroundModular evolution of secretion systems and virulence plasmids in a bacterial species complexPreprint
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. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.20.444927 · Cited by 3
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“Evolutionary processes are not always represented well by tree-like models, as hybridization, horizontal gene transfer, and other reticulate events often give rise to more complex structures [8, 24].”
WITHDRAWN: Antibiotic resistance in Pseudomonas aeruginosa – mechanisms, epidemiology and evolution
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Sapoval, N., Tanevski, M., & Treangen, T. J. (2023) · Pacific Symposium on Biocomputing (PSB) · doi:10.1142/9789811286421_0039 · Cited by 2
“Genomic repeats arising from horizontal gene transfer or duplication events have been associated with bacterial adaptation and evolution [18-20], functional diversification [20], and pathogenesis [18].”
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Nandy, M., Krishnaswamy, M., Sharda, M., & Seshasayee, A. S. N. (2025) · Journal of Molecular Biology · doi:10.1016/j.jmb.2025.169177 · Cited by 2
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“S10, S11, S12 and S13) was consistent with previous studies that demonstrated that xenologs are the main source of biochemical diversity used by prokaryotes to adapt to specific environments (Pál et al. 2005b; Treangen and Rocha 2011).”
ResultHorse Chestnut Bleeding Canker: A Twenty-First Century Tree Pathogen
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“Since genomic studies have demonstrated that genetic material is often transfered between organisms in a non-reproductive manner [3, 22], it has been commonly accepted that phylogenetic networks are more suitable than phylogenetic trees for modeling horizontal gene transfer, introgression, recombination and hybridizat…”
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“Horizontal gene transfer (HGT) is ubiquitous amongst prokaryotes (Treangen and Rocha 2011) and frequently underpins the colonization of new niches via metabolic innovation (Hehemann et al. 2016; Gogarten and Townsend 2005; Pál et al. 2005).”
BackgroundLinear-Time Tree Containment in Phylogenetic NetworksPreprint
Weller, M. (2017) · arXiv (Cornell University) · doi:10.48550/arxiv.1702.06364 · Cited by 2
“The use of DNA also gave strong support to the realization that trees are not always suited to display ancestral relations, as they fail to model recombination events such as hybridization (occurring frequently in plants) and horizontal gene transfer (a dominating factor in bacterial evolution) [5, 21].”
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“Less complex organisms, such as prokaryotes, may have evolved predominantly through other genetic mechanisms, e.g. horizontal gene transfer Treangen and Rocha (2011).”
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“There are also other mechanisms that have allowed the proteins to increase their diversity, such as gene splicing, duplication, and horizontal gene transfer, and versatility through intrinsically disordered proteins (Brites et al. 2013; Kondrashov and Koonin 2001; Schad et al. 2011; Treangen and Rocha 2011).”
BackgroundFunctional Genomic Characteristics of Marine Sponge-Associated Microbulbifer spongiae MI-GT
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tMHG-Finder: Tree-Guided Maximal Homologous Group Finder for Bacterial Genomes
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“In bacteria, gene family expansion mostly occurs through HGT rather than gene duplication [47], and this could provide a mechanism to ameliorate conflict between additional gene copies through the arrival of sub-functionalised genes directly.”
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Evolution of the Genomic Universe
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Microbial evolutionary reconstruction in the presence of mosaic sequences
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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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