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Horizontal gene transfer in evolution: facts and challenges
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The contribution of horizontal gene transfer to evolution has been controversial since it was suggested to be a force driving evolution in the microbial world. In this paper, I review the current standpoint on horizontal gene transfer in evolutionary thinking and discuss how important horizontal gene transfer is in evolution in the broad sense, and particularly in prokaryotic evolution. I review recent literature, asking, first, which processes are involved in the evolutionary success of transferred genes and, secondly, about the extent of horizontal gene transfer towards different evolutionary times. Moreover, I discuss the feasibility of reconstructing ancient phylogenetic relationships in the face of horizontal gene transfer. Finally, I discuss how horizontal gene transfer fits in the current neo-Darwinian evolutionary paradigm and conclude there is a need for a new evolutionary paradigm that includes horizontal gene transfer as well as other mechanisms in the explanation of evolution.
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“Increased copper tolerance was reported to be mediated by a genomic amplification of CUP1, decreased basal levels of the copper transporters CTR2 and CCC2 and decreased activity of antioxidant enzymes [117,128].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [117]
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BackgroundBraga, L. P. P., Soucy, S. M., Amgarten, D., da Silva, A. M., & Setúbal, J. C. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00006 · Cited by 49
“…by HGT, and generally, no two gene families, including 16S rDNA, share the same exact evolutionary history (Doolittle, 1999; Koonin et al., 2001; Gogarten and Townsend, 2005; Gribaldo and Brochier, 2009; Zhaxybayeva, 2009; Boto, 2010; Andam and Gogarten, 2011; Zhaxybayeva and Doolittle, 2011).”
BackgroundOrtiz‐Álvarez, R., Rı́os, A. D. L., Fernández‐Mendoza, F., Torralba‐Burrial, A., & Pérez-Ortega, S. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132718 · Cited by 47
“Incongruences appear from gene duplication, gene losses, horizontal gene transfers or incomplete lineage sorting [86,87].”
BackgroundParallel evolution of genome structure and transcriptional landscape in the Epsilonproteobacteria
Porcelli, I., Reuter, M., Pearson, B. M., Wilhelm, T. E., & van Vliet, A. H. M. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-616 · Cited by 44
“; licensee BioMed Central Commons Attribution License (http://creativec reproduction in any medium, provided the or genome, through combinations of gene inversion, recombination, gene duplication, deletion and horizontal gene transfer [3,4].”
BIOLOGICAL TAXONOMY AND ONTOLOGY DEVELOPMENT: SCOPE AND LIMITATIONS
Franz, N. M., & Thau, D. (2010) · Biodiversity Informatics · doi:10.1038/npre.2010.4593.1 · Cited by 46
Palmer, M., Steenkamp, E. T., Coetzee, M. P. A., Chan, W.-Y., van Zyl, E., Maayer, P. D., Coutinho, T. A., Blom, J., Smits, T. H. M., Duffy, B., et al. (2017) · Antonie van Leeuwenhoek · doi:10.1007/s10482-017-0852-4 · Cited by 47
“Despite the fact that horizontal gene transfer (HGT) significantly impacts the evolution of most, if not all, bacterial groups (Woese 2000; Gogarten et al. 2002; Jain et al. 2002; Boto 2010; Cohen et al. 2011), it is now possible to infer trees that trace the shared ancestry among all the species of a genus using WGS…”
BackgroundGeorgakopoulos-Soares, I., Yizhar-Barnea, O., Mouratidis, I., Hemberg, M., & Ahituv, N. (2020) · Genome Biology · doi:10.1186/s13059-021-02459-z · Cited by 46
Antarctic DNA moving forward: genomic plasticity and biotechnological potential
Martínez-Rosales, C., Fullana, N., Musto, H., & Castro‐Sowinski, S. (2012) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2012.02531.x · Cited by 43
Comparative Genomics of Nitrogen Cycling Pathways in Bacteria and Archaea
Albright, M., Timalsina, B., Martiny, J. B. H., & Dunbar, J. (2018) · Microbial Ecology · doi:10.1007/s00248-018-1239-4 · Cited by 46
Exploration of space to achieve scientific breakthroughs
Prasad, B., Richter, P. R., Vadakedath, N., Mancinelli, R. L., Krüger, M., Strauch, S. M., Grimm, D. G., Darriet, P., Chapel, J., Cohen, J., et al. (2020) · Biotechnology Advances · doi:10.1016/j.biotechadv.2020.107572 · Cited by 46
Identifying Drivers of Parallel Evolution: A Regression Model Approach
Bailey, S. F., Guo, Q., & Bataillon, T. M. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy210 · Cited by 42
“However, rates of HGT tend to be higher in bacteria, and in particular E. coli, as compared to yeast and other eukaryotes (e.g. Boto 2010).”
BackgroundHow the space environment influences organisms: an astrobiological perspective and review
Prasad, B., Richter, P. R., Vadakedath, N., Haag, F. W. M., Strauch, S. M., Mancinelli, R. L., Schwarzwälder, A., Etcheparre, E., Gaume, N., & Lebert, M. (2021) · International Journal of Astrobiology · doi:10.1017/s1473550421000057 · Cited by 46
“…yield, shorter growth period, flower colour, temperature tolerance, pathogen-resistance, etc. (Mei et al ., 1998; Cyranoski, 2001; Okamura et al ., 2003; Yamaguchi et al ., 2003, 2010; Wei et al ., 2006; Zhou et al ., 2006b; Li et al ., 2007; Chengzhi, 2011; Wong et al ., 2016; Yamaguchi, 2018).”
Evidence of horizontal gene transfer by transposase gene analyses in Fervidobacterium species
Cuecas, A., Kanoksilapatham, W., & Grau, J. M. G. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173961 · Cited by 41
Uhrig, R. G., Kerk, D., & Moorhead, G. B. G. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.224378 · Cited by 38
“One of the hallmarks of this process is a “discordant” clustering of sequences from distant organismal sources in the same gene tree (Keeling and Palmer, 2008; Boto, 2010).”
BackgroundDalquen, D. A., Altenhoff, A., Gonnet, G. H., & Dessimoz, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056925 · Cited by 39
“While exact numbers are still debated, it has been argued that the cumulative effect of LGT could be as high as 80 percent [28,29].”
Detecting horizontal gene transfer by mapping sequencing reads across species boundaries
Trappe, K., Marschall, T., & Renard, B. Y. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw423 · Cited by 38
Comparative Genomics Analysis of Lactobacillus mucosae from Different Niches
Jia, Y., Yang, B. K., Ross, R. P., Stanton, C., Zhang, H., Zhao, J., & Chen, W. (2020) · Genes · doi:10.3390/genes11010095 · Cited by 42
“In addition, transpositions have occurred at different positions of the CRISPR locus while transposases were associated with the frequent HGT in prokaryotes and had huge impacts on bacterial adaptation [70].”
BackgroundThe Microplastic-Antibiotic Resistance Connection
Marathe, N. P., & Bank, M. S. (2021) · Environmental contamination remediation and management · doi:10.1007/978-3-030-78627-4_9 · Cited by 41
Zheng, J., Peng, D., Ruan, L., & Sun, M. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-262 · Cited by 40
“Background Horizontal gene transfer (HGT) is the major driving force of bacterial evolution [1].”
The Quest for a Universal Theory of Life
Cleland, C. E. (2019) · Cambridge University Press eBooks · doi:10.1017/9781139046893 · Cited by 127
de la Cruz-Perera, C. I., Ren, D., Blanchet, M., Dendooven, L., Marsch, R., Sørensen, S. J., & Burmølle, M. (2012) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12036 · Cited by 39
“Plasmids are one of the key vectors of HTG, enabling genetic exchange between bacterial cells across species and domain barriers (Poole, 2009; Boto, 2010), and they very often encode genes that confer adaptive traits to their host, such as antibiotic resistance, biodegradation pathways and virulence (de la Cruz & Davi…”
BackgroundGómez-Valero, L., & Buchrieser, C. (2019) · Genes and Immunity · doi:10.1038/s41435-019-0074-z · Cited by 39
Kim, M., Cha, I., Lee, K., Li, M., & Park, S.-J. (2023) · Microbiology Spectrum · doi:10.1128/spectrum.01003-23 · Cited by 41
“Only 279 HGT events were detected in the genus and species (Table S6 and Fig.”
BackgroundInfluentialLemaire, B., Cauwenberghe, J. V., Chimphango, S. B. M., Stirton, C. H., Honnay, O., SMETS, E. F., & Muasya, A. M. (2015) · FEMS Microbiology Ecology · doi:10.1093/femsec/fiv118 · Cited by 38
Horizontally Acquired Genes Are Often Shared between Closely Related Bacterial Species
Bolotin, E., & Hershberg, R. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.01536 · Cited by 39
“Gene gain is a major driving force in the evolution of bacterial genomes (Ochman et al., 2000; Gogarten et al., 2002; Thomas and Nielsen, 2005; Boto, 2010; Vogan and Higgs, 2011; Arber, 2014).”
BackgroundInfluentialExperimental determination of evolutionary barriers to horizontal gene transfer
Kirit, H. A., Lagator, M., & Bollback, J. P. (2020) · BMC Microbiology · doi:10.1186/s12866-020-01983-5 · Cited by 34
“Yet, despite most transfer events resulting in fitness costs, HGT is still one of the major sources of novel genetic material in microbes (Boto, 2010; Soucy et al., 2015).”
BackgroundBhandari, V., Naushad, H. S., & Gupta, R. S. (2012) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2012.00098 · Cited by 35
“To account for the above observations and the occurrences of LGTs, it has been suggested that the prokaryotic evolution has both tree-like (at intermediate phylogenetic depths) and non-tree (or net-like) (at the base and tips) characteristics (Dagan et al., 2008; Puigbo et al., 2009, 2010; Swithers et al., 2009; Boto,…”
BackgroundMethodInfluentialHorizontal transfer of DNA methylation patterns into bacterial chromosomes
Shin, J.-E., Lin, C., & Lim, H. N. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw230 · Cited by 33
Katz, L. A. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2014.0324 · Cited by 33
Metadata
- Authors
- Boto, L.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Corresponding author
- Boto, Luis
- ORCID
- Boto, Luis
- Venue
- Proceedings of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2009-11-28
- Volume
- 277
- Issue
- 1683
- Pages
- 819-827
- ISSN
- 0080-4649 (ISSN-L)
- 0962-8452
- 1471-2954
- PMC
- PMC2842723
- OpenAlex
- W2108923274
- Cited by
- 379
- References
- 123
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 21 · 2023: 17 · 2022: 18 · 2021: 34 · 2020: 24 · 2019: 35 · 2018: 25 · 2017: 21 · 2016: 27 · 2015: 19 · 2014: 28 · 2013: 29 · 2012: 27
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the Royal Society B Biological Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy of Biology and Scientific Explanation
- Keywords
- horizontal gene transfer, prokaryotic evolution, microbial evolution, phylogenetic inference, evolutionary processes, evolutionary timescales
- MeSH terms
- Archaea, Bacteria, Biological Evolution, Phylogeny, Gene Transfer, Horizontal
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