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 indicates that HGT is the principal factor in microbial adaptation and innovation.
“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]
The Results report that HGT accounts for 88–98% of protein-family expansions in the prokaryotic clades studied. The Discussion says transferred genes can provide advantageous new functions, but hedges that transfer “might” account for most long-term adaptive protein-family expansions. That does not establish HGT as the principal factor in microbial adaptation and innovation generally. (LLM, conf=0.86)
Experimental — accuracy not yet measuredHorizontal gene transfer remained a key factor of microbial evolution and apparently a condition for long-term survival of microbial populations.
“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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MethodSelf-citationErosion of interaction networks in reduced and degraded genomes
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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.”
BackgroundSelf-citationHorizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli
Price, M. N., Dehal, P., & Arkin, A. P. (2008) · Genome biology · doi:10.1186/gb-2008-9-1-r4 · Cited by 1 · cited 1× · see citing works
“This picture is in agreement with the frequently observed co-transfer of transcription factors and their target genes [52], and”
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Horizontal gene transfer: building the web of life
Soucy, S. M., Huang, J.-L., & Gogarten, J. (2015) · Nature reviews genetics · doi:10.1038/nrg3962 · Cited by 1,304 · see citing works
Transposable Elements, Epigenetics, and Genome Evolution
Fedoroff, N. V. (2012) · Science · doi:10.1126/science.338.6108.758 · Cited by 634 · see citing works
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 561 · see citing works
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 · see citing works
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 · see citing works
Why prokaryotes have pangenomes
McInerney, J. O., McNally, A., & O’Connell, M. J. (2017) · Nature Microbiology · doi:10.1038/nmicrobiol.2017.40 · Cited by 403 · see citing works
Exploring the costs of horizontal gene transfer
Baltrus, D. A. (2013) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2013.04.002 · Cited by 398 · see citing works
Oliveira, P. H., Touchon, M., & Rocha, E. P. C. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku734 · Cited by 354 · see citing works
“Larger genomes are expected to follow the same general trend within bacteria (2).”
BackgroundSelf-citationConjugative and mobilizable genomic islands in bacteria: evolution and diversity
Bellanger, X., Payot, S., Leblond‐Bourget, N., & Guédon, G. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12058 · Cited by 372 · see citing works
The interaction between cyanobacteria and zooplankton in a more eutrophic world
Ger, K. A., Urrutia‐Cordero, P., Frost, P. C., Hansson, L., Sarnelle, O., Wilson, A. E., & Lürling, M. (2016) · Harmful Algae · doi:10.1016/j.hal.2015.12.005 · Cited by 352 · see citing works
“in cyanobacteria, selective forces operating on toxin producing genes such as the mcy complex may be overridden (Treangen and Rocha, 2011), likely resulting in weak grazer selection for toxin production in cyanobacteria compared to eukaryotic toxic”
BackgroundEndosymbiotic origin and differential loss of eukaryotic genes
Ku, C., Sathi, S. N., Roettger, M., Sousa, F. L., Lockhart, P. J., Bryant, D., Hazkani‐Covo, E., McInerney, J. O., Landan, G., & Martin, W. F. (2015) · Nature · doi:10.1038/nature14963 · Cited by 346 · see citing works
McHardy, I. H., Goudarzi, M., Tong, M., Ruegger, P. M., Schwager, E., Weger, J. R., Graeber, T. G., Sonnenburg, J. L., Horvath, S., Huttenhower, C., et al. (2013) · Microbiome · doi:10.1186/2049-2618-1-17 · Cited by 316 · see citing works
“[48-50].”
Bruto, M., Prigent‐Combaret, C., Muller, D. A. E., & Moënne‐Loccoz, Y. (2014) · Scientific Reports · doi:10.1038/srep06261 · Cited by 310 · see citing works
Czech, L., Hermann, L., Stöveken, N., Richter, A. A., Hoeppner, A., Smits, S. H. J., Heider, J., & Bremer, E. (2018) · Genes · doi:10.3390/genes9040177 · Cited by 294 · see citing works
“Lateral gene transfer is a major driver of microbial evolution [223,224] and has in particular shaped the genome of Archaea that acquired many genes from bacterial donors [225].”
BackgroundReal-Time Evolution of New Genes by Innovation, Amplification, and Divergence
Näsvall, J., Sun, L., Roth, J. R., & Andersson, D. I. (2012) · Science · doi:10.1126/science.1226521 · Cited by 282 · see citing works
PPanGGOLiN: Depicting microbial diversity via a partitioned pangenome graph
Gautreau, G., Bazin, A., Gachet, M., Planel, R., Burlot, L., Dubois, M., Perrin, A., Médigue, C., Calteau, A., Cruveiller, S., et al. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007732 · Cited by 282 · see citing works
“Most of these genes are acquired by horizontal gene transfer (HGT) [3].”
Self-citationGenomes in turmoil: quantification of genome dynamics in prokaryote supergenomes
Puigbò, P., Lobkovsky, A. E., Kristensen, D. M., Wolf, Y. I., & Koonin, E. V. (2014) · BMC Biology · doi:10.1186/s12915-014-0066-4 · Cited by 232 · see citing works
“Furthermore, evidence has been presented that HGT rather than gene duplication is the principal contributor to the evolution of gene families in prokaryotes [57].”
BackgroundTrichodesmium – a widespread marine cyanobacterium with unusual nitrogen fixation properties
Bergman, B., Sandh, G., Lin, S., Larsson, J., & Carpenter, E. J. (2012) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2012.00352.x · Cited by 268 · see citing works
“…and capacities when needed (e.g. via horizontal gene transfer, HGT) and maintain gene duplications (in-paralogs) affecting c. 10% of all genes in the Trichodesmium IMS101 genome, as a mechanism to promote genome expansion and organismal adaptations (Swingley et al., 2008; Treangen & Rocha, 2011).”
BackgroundComputational methods for Gene Orthology inference
Kristensen, D. M., Wolf, Y. I., Mushegian, A. R., & Koonin, E. V. (2011) · Briefings in Bioinformatics · doi:10.1093/bib/bbr030 · Cited by 249 · see citing works
“gene transfer (HGT) is a major component of the evolution of these organisms [39–45], so that their evolutionary history has to be represented by graphs that include not only vertical but also horizontal branches; algorithms for mapping of speciation and gene duplication events in such complex graphs are still unavail…”
BackgroundUnderstanding cyanobacteria‐zooplankton interactions in a more eutrophic world
Ger, K. A., Hansson, L., & Lürling, M. (2014) · Freshwater Biology · doi:10.1111/fwb.12393 · Cited by 239 · see citing works
“In fact, the latter may be the dominant driver of peptide evolution and diversity in prokaryotes, including cyanobacterial toxins (Treangen & Rocha, 2011).”
BackgroundInteractions in the microbiome: communities of organisms and communities of genes
Boon, E., Meehan, C. J., Whidden, C., Wong, D. H.-J., Langille, M. G. I., & Beiko, R. G. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12035 · Cited by 227 · see citing works
Sathi, S. N., Dagan, T., Landan, G., Janssen, A., Steel, M., McInerney, J. O., Deppenmeier, U., & Martin, W. F. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209119109 · Cited by 222 · see citing works
“2B), the simplest interpretation of monophyly for the 1,089 imports is that their origin traces to a single acquisition in the haloarchaeal common ancestor followed mainly by vertical descent and widespread differential loss, with some subsequent LGT among haloarchaea (21, 32, 33), notably for multicopy genes (34), no…”
BackgroundThe chromosomal organization of horizontal gene transfer in bacteria
Oliveira, P. H., Touchon, M., Cury, J., & Rocha, E. P. C. (2017) · Nature Communications · doi:10.1038/s41467-017-00808-w · Cited by 225 · see citing works
Self-citationOrigin and Evolution of the Universal Genetic Code
Koonin, E. V., & Novozhilov, A. S. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024713 · Cited by 200 · see citing works
Bacterial Sphingomyelinases and Phospholipases as Virulence Factors
Flores-Dı́az, M., Monturiol‐Gross, L., Naylor, C. E., Alape‐Girón, A., & Flieger, A. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00082-15 · Cited by 208 · see citing works
“According to the latter, horizontal gene transfer is recognized as playing a substantial role in the adaptive expansion of many protein families during prokaryotic genome evolution (12, 13).”
BackgroundFouz, N., Pangesti, K. N. A., Yasir, M., Al‐Malki, A. L., Azhar, E. I., Hill-Cawthorne, G. A., & Ghany, M. A. E. (2020) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed5010033 · Cited by 208 · see citing works
“The situation of ARGs is more complex, because they are not degradable and can be spread among microbial communities in the environment through horizontal gene transfer, which is the main resistance mechanism in Enterobacteriaceae [33,34].”
BackgroundOn the evolution of bacterial multicellularity
Lyons, N. A., & Kolter, R. (2015) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.12.007 · Cited by 202 · see citing works
“Current Opinion in Microbiology 2015, 24:21–28 microbial world, which some have suggested may play a bigger role in bacterial evolution than classic mechanisms like gene duplication [55].”
Potential Effects of Horizontal Gene Exchange in the Human Gut
Lerner, A., Matthias, T., & Aminov, R. I. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01630 · Cited by 200 · see citing works
“In general, HGT drives the enlargement of protein families in bacteria and archaea to deal with the environmental and anthropogenic impacts imposed upon them (19).”
BackgroundThe last universal common ancestor between ancient Earth chemistry and the onset of genetics
Weiss, M. C., Preiner, M., Xavier, J. C., Zimorski, V., & Martin, W. F. (2018) · PLOS Genetics · doi:10.1371/journal.pgen.1007518 · Cited by 186 · see citing works
Regulation of genetic flux between bacteria by restriction–modification systems
Oliveira, P. H., Touchon, M., & Rocha, E. P. C. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603257113 · Cited by 166 · see citing works
“Larger bacterial genomes are expected to engage in more frequent HGT because this is the dominant mechanism of genetic accretion (28).”
BackgroundSelf-citationGenomic diversity of 2010 Haitian cholera outbreak strains
Hasan, N. A., Choi, S. Y., Eppinger, M., Clark, P. W., Chen, A., Alam, M., Haley, B. J., Taviani, E., Hine, E., Su, Q., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207359109 · Cited by 189 · see citing works
“Thus, within a dynamic microbial gene pool, in which horizontal gene transfer is a significant driver of microbial evolution (16), MGEs play a pivotal role in the genesis of diversity and hypervariability of Vibrio genomes (14, 15).”
BackgroundInfluentialThiergart, T., Landan, G., Schenk, M., Dagan, T., & Martin, W. F. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs018 · Cited by 170 · see citing works
Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution
Schönknecht, G., Weber, A. P. M., & Lercher, M. J. (2013) · BioEssays · doi:10.1002/bies.201300095 · Cited by 165 · see citing works
Antimicrobials and Antibiotic Resistance Genes in Water Bodies: Pollution, Risk, and Control
Singh, A. K., Kaur, R., Verma, S., & Singh, S. (2022) · Frontiers in Environmental Science · doi:10.3389/fenvs.2022.830861 · Cited by 165 · see citing works
Genome fluctuations in cyanobacteria reflect evolutionary, developmental and adaptive traits
Larsson, J., Nylander, J. A. A., & Bergman, B. (2011) · BMC Evolutionary Biology · doi:10.1186/1471-2148-11-187 · Cited by 164 · see citing works
“Additionally, gene transfers both within cyanobacteria and from other phyla have been reported previously [51-53] and may contribute substantially to the expansion of gene families [54].”
BackgroundKoonin, E. V. (2016) · F1000Research · doi:10.12688/f1000research.8737.1 · Cited by 152 · see citing works
McDowell, A., Nagy, I., Magyari, M., Barnard, E., & Patrick, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070897 · Cited by 149 · see citing works
“One very recent study has, however, challenged this view and suggested that expansion of gene families in bacteria via HGT and incomplete xenologous gene replacement may be much more important than first thought [60].”
BackgroundInfluentialKu, C., & Martin, W. F. (2016) · BMC Biology · doi:10.1186/s12915-016-0315-9 · Cited by 147 · see citing works
“that prokaryotes generate diversity mainly through acquisition, rather than through duplication [31].”
BackgroundRates of Lateral Gene Transfer in Prokaryotes: High but Why?
Vos, M., Hesselman, M. C., Beek, T. A. H. T., van Passel, M. W. J., & Eyre‐Walker, A. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.07.006 · Cited by 147 · see citing works
Models, algorithms and programs for phylogeny reconciliation
Doyon, J., Ranwez, V., Daubin, V., & Berry, V. (2011) · Briefings in Bioinformatics · doi:10.1093/bib/bbr045 · Cited by 142 · see citing works
“The development of such models is crucial to gain insight into the evolution of unicellular organisms where LGT has played a major role [2] and, more generally, to clarify homology relationships among genes.”
BackgroundMaddamsetti, R., Yao, Y., Wang, T., Gao, J., Huang, V. T., Hamrick, G. S., Son, H.-I., & You, L. (2024) · Nature Communications · doi:10.1038/s41467-024-45638-9 · Cited by 142 · see citing works
Fungal metabolic gene clusters—caravans traveling across genomes and environments
Wisecaver, J. H., & Rokas, A. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00161 · Cited by 128 · see citing works
Takeuchi, N., Kaneko, K., & Koonin, E. V. (2014) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.113.009845 · Cited by 125 · see citing works
Remigi, P., Anisimova, M. O., Guidot, A., Genin, S., & Peeters, N. M. (2011) · New Phytologist · doi:10.1111/j.1469-8137.2011.03854.x · Cited by 123 · see citing works
Pan-genome analyses of model fungal species
McCarthy, C. G. P., & Fitzpatrick, D. A. (2019) · Microbial Genomics · doi:10.1099/mgen.0.000243 · Cited by 122 · see citing works
“These results appear to indicate that gene duplication, which is the driving factor of gene family expansion in eukaryotes, does play an important role in the evolution of fungal accessory genomes (and pangenomes as a whole) [95, 96].”
Horizontal Gene Transfer and the History of LifePreprint
Daubin, V., & Szöllősi, G. J. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018036 · Cited by 122 · see citing works
Aharon, Y., Pasternak, Z., Ben‐Yosef, M., Behar, A., Lauzon, C. R., Yuval, B., & Jurkevitch, É. (2012) · Applied and Environmental Microbiology · doi:10.1128/aem.02761-12 · Cited by 117 · see citing works
“Enterobacteriaceae (48) and enhanced in dense populations.”
Testing the Infinitely Many Genes Model for the Evolution of the Bacterial Core Genome and Pangenome
Collins, R. E., & Higgs, P. G. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/mss163 · Cited by 116 · see citing works
Interbacterial predation as a strategy for DNA acquisition in naturally competent bacteria
Veening, J., & Blokesch, M. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.66 · Cited by 115 · see citing works
Phylogenomic networks reveal limited phylogenetic range of lateral gene transfer by transduction
Popa, O., Landan, G., & Dagan, T. (2016) · The ISME Journal · doi:10.1038/ismej.2016.116 · Cited by 112 · see citing works
“Transduction within the lineage may thus contribute to protein family expansion in bacteria, which was proposed to be mediated more often by LGT than by gene duplication (Hooper and Berg, 2003; Treangen and Rocha, 2011).”
Evidence for horizontal transfer of mitochondrial DNA to the plastid genome in a bamboo genus
Ma, P., Zhang, Y., Guo, Z., & Li, D.-Z. (2015) · Scientific Reports · doi:10.1038/srep11608 · Cited by 110 · see citing works
Beyond 16S rRNA Community Profiling: Intra-Species Diversity in the Gut Microbiota
Ellegaard, K., & Engel, P. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01475 · Cited by 110 · see citing works
“However, unlike multi-cellular eukaryotes, bacterial evolution is also strongly influenced by horizontal gene transfer (Ochman et al., 2000; Treangen and Rocha, 2011; Koskella and Vos, 2015).”
BackgroundInevitability of Genetic Parasites
Iranzo, J., Puigbò, P., Lobkovsky, A. E., Wolf, Y. I., & Koonin, E. V. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw193 · Cited by 90 · see citing works
“Horizontal gene transfer (HGT) is a dominant process in the evolution of bacteria and archaea that is the source of most innovations and adaptations to new environments (Lerat et al. 2005; Dagan et al. 2008; Koonin and Wolf 2008; Treangen and Rocha 2011; Puigbo et al. 2014).”
BackgroundEcosystems biology of microbial metabolism
Klitgord, N., & Segrè, D. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.04.018 · Cited by 102 · see citing works
Relaxosome function and conjugation regulation in F‐like plasmids – a structural biology perspective
Wong, J. J. W., Lu, J., & Glover, J. N. M. (2012) · Molecular Microbiology · doi:10.1111/j.1365-2958.2012.08131.x · Cited by 102 · see citing works
“17% to 25% of the Escherichia coli genome is thought to originate from horizontal gene transfer (Narra and Ochman, 2006), which has recently shown to be responsible for protein family expansion in 88–98% of genes across eight genetically distant bacterial clades (Treangen and Rocha, 2011).”
BackgroundThe Timetree of Prokaryotes: New Insights into Their Evolution and Speciation
Marin, J., Battistuzzi, F. U., Brown, A. C., & Hedges, S. B. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw245 · Cited by 101 · see citing works
Deschamps, P., Zivanovic, Y., Moreira, D., Rodríguez‐Valera, F., & López‐García, P. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu127 · Cited by 100 · see citing works
“HGT is an important force in evolution, contributing to innovation and adaptation to changing or new environments through the expansion of gene families and the import of radically different metabolic functions (Ochman et al. 2000; Gogarten et al. 2002; Treangen and Rocha 2011).”
BackgroundGupta, R. S. (2016) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuw011 · Cited by 97 · see citing works
“…a sizeable fraction of genes/proteins (often one-third or more of the total genome) in different prokaryotic genomes are unique showing no similarity to other gene/protein in the databases (Danchin 2003; Siew and Fischer 2003; Daubin and Ochman 2004; Tettelin et al. 2005; Treangen and Rocha 2011).”
BackgroundGenomic language model predicts protein co-regulation and function
Hwang, Y., Cornman, A. L., Kellogg, E. H., Ovchinnikov, S., & Girguis, P. R. (2024) · Nature Communications · doi:10.1038/s41467-024-46947-9 · Cited by 99 · see citing works
Microbial Evolution: Towards Resolving the Plasmid Paradox
MacLean, R. C., & Millán, Á. S. (2015) · Current Biology · doi:10.1016/j.cub.2015.07.006 · Cited by 92 · see citing works
Chen, S., Sun, G., Rosen, B. P., Zhang, S., Deng, Y., Zhu, B., Rensing, C., & Zhu, Y. (2017) · Scientific Reports · doi:10.1038/s41598-017-08313-2 · Cited by 93 · see citing works
Networks of lexical borrowing and lateral gene transfer in language and genome evolution
List, J., Sathi, S. N., Geisler, H., & Martin, W. F. (2013) · BioEssays · doi:10.1002/bies.201300096 · Cited by 89 · see citing works
“In prokaryotes, gene families arise via the acquisition of related sequences through lateral gene transfer, not through duplication [56].”
BackgroundMolecular epidemiology and genomics of group A Streptococcus
Bessen, D. E., McShan, W. M., Nguyen, S. V., Shetty, A. C., Agrawal, S., & Tettelin, H. (2014) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2014.10.011 · Cited by 89 · see citing works
“The latter is a form of replacing HGT. Analysis of 17 Streptococcus genomes, of which 12 are GAS, reveals that HGT of orthologs far outweighs the contribution of gene duplication to the expansion and diversification of gene families (Treangen and Rocha, 2011).”
Archaeal and eukaryotic homologs of Hfq
Mura, C., Randolph, P. S., Patterson, J. A. K., & Cozen, A. E. (2013) · RNA Biology · doi:10.4161/rna.24538 · Cited by 87 · see citing works
Li, M., Zhao, J., Tang, N., Sun, H., & Huang, J. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00701 · Cited by 85 · see citing works
“In prokaryotic genomes, transferred genes are responsible for the majority of protein families’ expansion (Treangen and Rocha, 2011).”
BackgroundJiang, X., Hall, A. B., Xavier, R. J., & Alm, E. J. (2019) · PLoS ONE · doi:10.1371/journal.pone.0223680 · Cited by 88 · see citing works
“Canonical classes of MGEs includes prophages[7], group II introns[8], and transposons[9].”
BackgroundA Bayesian Method for Analyzing Lateral Gene Transfer
Sjöstrand, J., Tofigh, A., Daubin, V., Arvestad, L., Sennblad, B., & Lagergren, J. (2014) · Systematic Biology · doi:10.1093/sysbio/syu007 · Cited by 84 · see citing works
Quantifying Homologous Replacement of Loci between Haloarchaeal Species
Williams, D. F., Gogarten, J. P., & Papke, R. T. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs098 · Cited by 85 · see citing works
“Given the relative rareness of paralogy to xenology in prokaryotes (Treangen and Rocha 2011; see also section Quartet Decomposition), it is most parsimonious to interpret highly supported discordant trees as evidence for HGT.”
BackgroundResultKoonin, E. (2017) · Life · doi:10.3390/life7020022 · Cited by 85 · see citing works
“Given that HGT, even if limited by both physical and selective barriers, remained a key factor of microbial evolution [36-40], and apparently, a condition for long term survival of microbial populations [41, 42], it stands to reason that it played a key role not only in the primordial universalization of the code but…”
BackgroundMerlo, M. A., Cross, I., Palazón-Fernández, J. L., Úbeda-Manzanaro, M., Sarasquete, C., & Rebordinos, L. G. (2012) · BMC Evolutionary Biology · doi:10.1186/1471-2148-12-201 · Cited by 83 · see citing works
“The HT phenomenon has been documented extensively in prokaryotes, and is a well-known mechanism of gene exchange [25]; it has been assumed that between 88% and 98% of the expansion of protein families in prokaryotes is due to HT [26].”
BackgroundThe Modern Synthesis in the Light of Microbial Genomics.
Booth, A., Mariscal, C., & Doolittle, W. (2016) · Annual Review of Microbiology · doi:10.1146/annurev-micro-102215-095456 · Cited by 65 · see citing works
“Indeed, it is now thought likely that, within prokaryotes, what appear to be duplications are more often the product of LGT events introducing orthologs from other strains or species (119).”
BackgroundGenomic evolution and adaptation of arthropod-associated Rickettsia
Karkouri, K. E., Ghigo, É., Raoult, D., & Fournier, P. (2022) · Scientific Reports · doi:10.1038/s41598-022-07725-z · Cited by 81 · see citing works
Alexander, W. G., Wisecaver, J. H., Rokas, A., & Hittinger, C. T. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517242113 · Cited by 82 · see citing works
MVP: a microbe–phage interaction database
Gao, N., Zhang, C., Zhang, Z., Hu, S., Lercher, M. J., Zhao, X., Peer Bork, B., Liu, Z., & Chen, W.-H. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1124 · Cited by 79 · see citing works
“In addition, lateral gene transfers frequently occur and contribute significantly to the expansion of gene repertoire in prokaryotes (48).”
BackgroundGene duplication drives genome expansion in a major lineage of Thaumarchaeota
Sheridan, P. O., Raguideau, S., Quince, C., Holden, J. M., Zhang, L., Gaze, W. H., Holden, J. M., Mead, A., Raguideau, S., Quince, C., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19132-x · Cited by 77 · see citing works
Ares-Arroyo, M., Coluzzi, C., & Rocha, E. P. C. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac1079 · Cited by 78 · see citing works
“Plasmids are extra-chromosomal DNA molecules that have an important role in horizontal gene transfer (1), being key contributors to the spread of antimicrobial resistance genes, virulence factors, and metabolic traits (2).”
BackgroundSelf-citationRemigi, P., Capela, D., Clérissi, C., Tasse, L., Torchet, R., Bouchez, O., Batut, J., Cruveiller, S., Rocha, E. P. C., & Masson‐Boivin, C. (2014) · PLoS Biology · doi:10.1371/journal.pbio.1001942 · Cited by 77 · see citing works
“HGT plays a ubiquitous role in the diversification of prokaryotes and exploration of new ecological niches [1,2].”
Self-citationHow enzyme promiscuity and horizontal gene transfer contribute to metabolic innovation
Glasner, M. E., Truong, D. P., & Morse, B. C. (2019) · FEBS Journal · doi:10.1111/febs.15185 · Cited by 77 · see citing works
Copy Number Change: Evolving views on Gene Amplification
Elliott, K. T., Cuff, L. E., & Neidle, E. L. (2013) · Future Microbiology · doi:10.2217/fmb.13.53 · Cited by 78 · see citing works
“Despite the challenge in detailed characterization, there is intensive interest in the role of intrachromosomal gene duplication in evolution [14,21,30].”
BackgroundResultInfluentialGlobal Patterns of Protein Domain Gain and Loss in Superkingdoms
Nasir, A., Kim, K. M., & Caetano‐Anollés, G. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003452 · Cited by 74 · see citing works
“Finally, changes to domain repertoires are also possible by HGT that is believed to occur with high frequency in microbial species, especially Bacteria [25,26].”
BackgroundTransfer of noncoding DNA drives regulatory rewiring in bacteria
Oren, Y., Smith, M. B., Johns, N. I., Zeevi, M. K., Biran, D., Ron, E. Z., Corander, J., Wang, H. H., Alm, E. J., & Pupko, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413272111 · Cited by 75 · see citing works
“These striking findings have led many to believe that changes in gene content underlie the rapid pace of bacterial evolution (5, 6).”
BackgroundMechanisms That Shape Microbial Pangenomes
Domingo-Sananes, M. R., & McInerney, J. O. (2021) · Trends in Microbiology · doi:10.1016/j.tim.2020.12.004 · Cited by 74 · see citing works
Coevolution of the Organization and Structure of Prokaryotic GenomesPreprint
Touchon, M., & Rocha, E. P. C. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018168 · Cited by 74 · see citing works
“2013), and acquisitions of new genes occur mostly by horizontal gene transfer (Treangen and Rocha 2011).”
BackgroundSelf-citationInter-phylum HGT has shaped the metabolism of many mesophilic and anaerobic bacteria
Caro‐Quintero, A., & Konstantinidis, K. T. (2014) · The ISME Journal · doi:10.1038/ismej.2014.193 · Cited by 73 · see citing works
Dmitrijeva, M., Tackmann, J., Matias Rodrigues, J. F., Huerta-Cepas, J., Coelho, L. P., & von Mering, C. (2024) · Nature Ecology & Evolution · doi:10.1038/s41559-024-02357-0 · Cited by 72 · see citing works
“Gene gain through horizontal gene transfer (HGT) in particular is a driving force in prokaryotic genome evolution 1,2 , and most genes have been shown to undergo HGT at least once in their evolutionary history 3,4 .”
BackgroundThe Extent of Genome Flux and Its Role in the Differentiation of Bacterial Lineages
Nowell, R. W., Green, S., Laue, B. E., & Sharp, P. M. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu123 · Cited by 71 · see citing works
“We demonstrate a history of extensive genome fluctuation for this species and show that individual lineages could have acquired thousands of genes in the same period in which a 1% amino acid divergence accrues in thecoregenome.”
BackgroundAn Emerging Mycoplasma Associated with Trichomoniasis, Vaginal Infection and Disease
Fettweis, J. M., Serrano, M. G., Huang, B., Brooks, J. P., Glascock, A. L., Sheth, N. U., Strauss, J. F., Jefferson, K. K., & Buck, G. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110943 · Cited by 70 · see citing works
“Although these organisms exhibit a low level of horizontal gene transfer, expanded families of surface proteins are an exception [43–45].”
BackgroundThe chromosomal accommodation and domestication of mobile genetic elements
Touchon, M., Bobay, L., & Rocha, E. P. C. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.09.010 · Cited by 70 · see citing works
Self-citationGrammar of protein domain architectures
Yu, L., Tanwar, D. K., Penha, E. D. D. S., Wolf, Y. I., Koonin, E. V., & Basu, M. K. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1814684116 · Cited by 68 · see citing works
The complex evolutionary history of aminoacyl-tRNA synthetases
Chaliotis, A., Vlastaridis, P., Mossialos, D., Ibba, M., Becker, H. D., Stathopoulos, C., & Amoutzias, G. D. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw1182 · Cited by 69 · see citing works
“This calculation is in accordance with previous large-scale analyses on other protein families, where HGT instead of intra-chromosomal gene duplication is considered the main driving force behind protein family expansion in prokaryotes with an estimated contribution of 88–98% (61).”
ResultAndreini, C., Rosato, A., & Banci, L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171279 · Cited by 69 · see citing works
The Ingenuity of Bacterial Genomes
Kirchberger, P. C., Schmidt, M. L., & Ochman, H. (2020) · Annual Review of Microbiology · doi:10.1146/annurev-micro-020518-115822 · Cited by 68 · see citing works
Early evolution without a tree of life
Martin, W. F. (2011) · Biology Direct · doi:10.1186/1745-6150-6-36 · Cited by 68 · see citing works
“In prokaryote genome evolution, lateral gene transfer (LGT) is an important mechanism of natural variation [4], while the prokaryote-to-eukaryote transition involved the wholesale merger of prokaryotic genomes via endosymbiosis [5-7].”
BackgroundAlienness: Rapid Detection of Candidate Horizontal Gene Transfers across the Tree of Life
Rancurel, C., Legrand, L., & Danchin, É. (2017) · Genes · doi:10.3390/genes8100248 · Cited by 68 · see citing works
Sitaraman, R. (2018) · Microbiome · doi:10.1186/s40168-018-0551-z · Cited by 67 · see citing works
Mao, M., Yang, X., & Bennett, G. M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1811932115 · Cited by 67 · see citing works
“Gene duplications are an important source of functional novelty in organismal adaptation (59, 60).”
BackgroundThe Turbulent Network Dynamics of Microbial Evolution and the Statistical Tree of Life
Koonin, E. V. (2015) · Journal of Molecular Evolution · doi:10.1007/s00239-015-9679-7 · Cited by 65 · see citing works
“Acquisition of new genes and whole suits of genes, such as operons, appears to be the principal way of expanding metabolic networks in microbes (Andersson 2009; Treangen and Rocha 2011).”
BackgroundPredictive microbiology theory and application: Is it all about rates?
McMeekin, T. A., Olley, J. N., Ratkowsky, D. A., Corkrey, R., & Ross, T. (2012) · Food Control · doi:10.1016/j.foodcont.2012.06.001 · Cited by 65 · see citing works
“Treangen and Rocha (2011) compared the roles of HGT and gene duplication showing that the vast majority of expansions in protein families are due to transfer.”
BackgroundGenome plasticity and systems evolution in Streptomyces
Zhou, Z. M., Gu, J., Li, Y.-Q., & Wang, Y. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-s10-s8 · Cited by 64 · see citing works
“LGT is particularly important for bacteria as it is a general mechanism for them to acquire genetic materials from other organisms via transformation, conjugation, bacterial phage transduction, and acquisition of plasmids [8,12-14].”
BackgroundAdaptation in Natural Microbial Populations
Koskella, B. L., & Vos, M. (2015) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-112414-054458 · Cited by 64 · see citing works
- 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 › Agricultural and Biological Sciences › Plant Science › 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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