The DOI matches its Crossref record; 75 of the 75 references it cites were found in a registry or an index.
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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Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · cited 7×
“OrthoMCL defines putative orthologous relationships between a pair of genomes as BLASTP reciprocal better/best hits.”
MethodInfluentialMUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · cited 1×
“Protein alignments were generated using MUSCLE [73] and then back-translated to DNA.”
MethodOrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
Li, L., Stoeckert, C. J., & Roos, D. S. (2003) · Genome Research · doi:10.1101/gr.1224503 · Cited by 5,707 · cited 2×
“OrthoMCL defines putative orthologous relationships between a pair of genomes as BLASTP reciprocal better/best hits.”
MethodPAML: a program package for phylogenetic analysis by maximum likelihood
Yang, Z. (1997) · Computer applications in the biosciences · doi:10.1093/bioinformatics/13.5.555 · Cited by 5,377 · cited 1×
“Non-synonymous (dN) and synonymous (dS) substitution rates in paralogs (blue; dashed linear fit) and xenologs (red; solid linear fit) in all clades computed using Codeml from PAML [76] (model = 1, fix_omega = 0).”
MethodSharp, P. M., & Li, W.-H. (1987) · Nucleic Acids Research · doi:10.1093/nar/15.3.1281 · Cited by 3,992 · cited 1×
“We first tested if the two classes of protein families have different gene expression levels using the codon adaptation index (CAI; [44]).”
MethodLateral gene transfer and the nature of bacterial innovation
Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000) · Nature · doi:10.1038/35012500 · Cited by 3,816 · cited 1×
“Horizontal gene transfer (HGT) results in the acquisition of radically new genetic information, liberating genomic evolutionary processes from tinkering exclusively with pre-existing genes”
BackgroundAn efficient algorithm for large-scale detection of protein families
Enright, A. J. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.7.1575 · Cited by 3,536 · cited 4×
“OrthoMCL defines putative orthologous relationships between a pair of genomes as BLASTP reciprocal better/best hits.”
MethodInfluentialISfinder: the reference centre for bacterial insertion sequences
Siguier, P. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj014 · Cited by 2,767 · cited 2×
“coli our databank contained all IS present in IS Finder [67].”
BackgroundTREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing
Schmidt, H. A., Strimmer, K., Vingron, M., & von Haeseler, A. (2002) · Bioinformatics · doi:10.1093/bioinformatics/18.3.502 · Cited by 2,512 · cited 1×
“Tree-Puzzle [74] was used to generate the matrix of distances by maximum likelihood with the HKY+C model and exact parameter estimates.”
MethodBIONJ: an improved version of the NJ algorithm based on a simple model of sequence data
Gascuel, O. (1997) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025808 · Cited by 1,850 · cited 2×
“The trees were then computed from these distance matrices using BIONJ [75].”
MethodInfluential
Research works printed but not linked: 1
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Cited by
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Horizontal gene transfer: building the web of life
Soucy, S. M., Huang, J., & Gogarten, J. P. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3962 · Cited by 1,530
Transposable Elements, Epigenetics, and Genome Evolution
Fedoroff, N. V. (2012) · Science · doi:10.1126/science.338.6108.758 · Cited by 634
Antibiotic resistance in Pseudomonas aeruginosa – Mechanisms, epidemiology and evolution
Botelho, J., Grosso, F., & Peixe, L. M. S. V. (2019) · Drug Resistance Updates · doi:10.1016/j.drup.2019.07.002 · Cited by 590
Stecher, B., Denzler, R., Maier, L., Bernet, F., Sanders, M. J., Pickard, D. J., Barthel, M., Westendorf, A. M., Krogfelt, K. A., Walker, A. W., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113246109 · Cited by 492
Gene Transfer from Bacteria and Archaea Facilitated Evolution of an Extremophilic Eukaryote
Schönknecht, G., Chen, W., Ternes, C. M., Barbier, G. G., Shrestha, R. P., Stanke, M., Bräutigam, A., Baker, B. J., Banfield, J. F., Garavito, R. M., et al. (2013) · Science · doi:10.1126/science.1231707 · Cited by 490
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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