Horizontal Gene Transfer Building Prokaryote Genomes: Genes Related to Exchange Between Cell and Environment are Frequently Transferred

Paquola, Apuã C. M.; Asif, Huma; Pereira, Carlos Alberto de Bragança; Feltes, Bruno César; Bonatto, Diego; Lima, Wanessa Cristina; Menck, Carlos Frederico Martins

doi:10.1007/s00239-018-9836-x

Original Article
Published: 19 March 2018

Horizontal Gene Transfer Building Prokaryote Genomes: Genes Related to Exchange Between Cell and Environment are Frequently Transferred

Apuã C. M. Paquola^1,2,
Huma Asif^1,3,
Carlos Alberto de Bragança Pereira⁴,
Bruno César Feltes^5,6,
Diego Bonatto⁵,
Wanessa Cristina Lima^1,7 &
Carlos Frederico Martins Menck¹

Journal of Molecular Evolution volume 86, pages 190–203 (2018)Cite this article

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Abstract

Horizontal gene transfer (HGT) has a major impact on the evolution of prokaryotic genomes, as it allows genes evolved in different contexts to be combined in a single genome, greatly enhancing the ways evolving organisms can explore the gene content space and adapt to the environment. A systematic analysis of HGT in a large number of genomes is of key importance in understanding the impact of HGT in the evolution of prokaryotes. We developed a method for the detection of genes that potentially originated by HGT based on the comparison of BLAST scores between homologous genes to 16S rRNA-based phylogenetic distances between the involved organisms. The approach was applied to 697 prokaryote genomes and estimated that in average approximately 15% of the genes in prokaryote genomes originated by HGT, with a clear correlation between the proportion of predicted HGT genes and the size of the genome. The methodology was strongly supported by evolutionary relationships, as tested by the direct phylogenetic reconstruction of many of the HGT candidates. Studies performed with Escherichia coli W3110 genome clearly show that HGT proteins have fewer interactions when compared to those predicted as vertical inherited, an indication that the number of protein partners imposes limitations to horizontal transfer. A detailed functional classification confirms that genes related to protein translation are vertically inherited, whereas interestingly, transport and binding proteins are strongly enriched among HGT genes. Because these genes are related to the cell exchange with their environment, their transfer most likely contributed to successful adaptation throughout evolution.

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Funding

This project received financial support from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brasília, DF, Brazil) and Comissão de Aperfeiçoamento do Ensino Superior (CAPES, Brasília, DF, Brazil) and Foundation for Research Support of the State of Sao Paulo (FAPESP, São Paulo, SP, Brazil).

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Affiliations

Department of Microbiology, Institute of Biomedical Sciences, University of Sao Paulo, Av. Prof. Lineu Prestes, 1374, São Paulo, SP, 05508-000, Brazil
Apuã C. M. Paquola, Huma Asif, Wanessa Cristina Lima & Carlos Frederico Martins Menck
Lieber Institute for Brain Development, Baltimore, MD, USA
Apuã C. M. Paquola
Department of Psychiatry and Behavioral Neurosciences, The University of Chicago, Chicago, IL, USA
Huma Asif
Department of Statistics, Institute of Mathematics and Statistics, University of Sao Paulo, São Paulo, Brazil
Carlos Alberto de Bragança Pereira
Center of Biotechnology, Department of Molecular Biology and Biotechnology, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil
Bruno César Feltes & Diego Bonatto
Institute of Informatics, Structural Bioinformatics and Computational Biology Laboratory, Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil
Bruno César Feltes
Department of Pharmacology, University of Heidelberg, Im Neuenheimer Feld 366, 69120, Heidelberg, Germany
Wanessa Cristina Lima

Authors

Apuã C. M. Paquola
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Huma Asif
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Carlos Alberto de Bragança Pereira
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Bruno César Feltes
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Diego Bonatto
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Wanessa Cristina Lima
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Carlos Frederico Martins Menck
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Contributions

AP, WL, and CM designed and developed the method. CM defined the strategy and supervised. HA, CP, BC, and DB analyzed the data. HA, AP, and CM wrote, discussed, and edited the manuscript. AP, HA, and BC prepared the figures. WL discussed and edited the manuscript.

Corresponding author

Correspondence to Carlos Frederico Martins Menck.

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The authors declare that they have no competing interests.

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Apuã C. M. Paquola and Huma Asif contributed equally to this manuscript.

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Paquola, A.C.M., Asif, H., Pereira, C.A.d.B. et al. Horizontal Gene Transfer Building Prokaryote Genomes: Genes Related to Exchange Between Cell and Environment are Frequently Transferred. J Mol Evol 86, 190–203 (2018). https://doi.org/10.1007/s00239-018-9836-x

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Received: 14 December 2017
Accepted: 15 March 2018
Published: 19 March 2018
Issue Date: April 2018
DOI: https://doi.org/10.1007/s00239-018-9836-x

Keywords

Horizontal gene transfer
Evolution
Phylogenetic tree incongruence
Transport proteins