Three recent papers underline the importance of the host genomic background in allowing the stable maintenance of horizontally acquired genes. These studies suggest that post-transfer changes in both host genome and acquired genes contribute to the stable integration of foreign genes.This study was supported by a Grant of Spanish DGI   (CGL2013-41375-P).Peer reviewe

Boto, Luis

Journal of Molecular Evolution

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1  ACCEPTING FOREIGN GENES 1  2 LUIS BOTO 3  4 Dpto. Biodiversidad y Biología Evolutiva. 5 Museo Nacional de Ciencias Naturales (CSIC) 6 C/ José Gutierrez Abascal 2 7 28006 Madrid 8 Spain 9 Phone: (34) 914111328 Ext 1131 10 Fax: (34) 915645078 11 e-mail: mcnb119@mncn.csic.es 12  13  14 Acknowledgements. 15 Author is supported by a grant of Spanish DGI (CGL2013-41375-P). Author thanks to 16 Elena Bulmer for English editing of the manuscript 17  18  19  20 Key words: Evolution, Horizontal gene transfer, integration of foreign genes, 21 contingency22 2   23 ABSTRACT: 24 Three recent papers underline the importance of the host genomic background in 25 allowing the stable maintenance of horizontally acquired genes. These studies suggest 26 that post-transfer changes in both, host genome and acquired genes contribute to the 27 stable integration of foreign genes. 28 29 3   30 In the last twenty five years horizontal gene transfer has been recognized as a 31 force modulating the evolution of bacterial, archaeal, unicellular eukaryotes, plants, 32 fungi  and, to a less extent, metazoan genomes, and consequently as a force that 33 modulates the evolution of the life on earth. A search in the Thompson Web of Science 34 using “horizontal gene transfer” as query yields more than ten new publications coming 35 out per week, which clearly reveals to us that this is an active research field. 36  Over the past twenty five years many genes have been identified as being 37 horizontally transferred between organisms. Moreover, insights in mechanisms that 38 allow the transfer and stable integration of foreign genes in the new genomic context 39 have been revealed. This includes for example the characterization of barriers that 40 horizontally acquired genes need to overcome to become integrated in the receptor 41 genomes (Thomas and Nielsen 2005; Baltrus 2013; Boto 2015). 42 However, the role performed by the recipient genetic background and the post-43 transfer responses in the stable integration of foreign genes has been hardly studied. 44 Three recent papers (Michener et al. 2014; Pascuan et al. 2015; Llorente et al. 2016) that 45 combine the identification of horizontally transferred genes  with experimental genetic 46 engineering approaches have shed light in this topic revealing that the assimilation of 47 foreign genes by an organism is contingent to the evolution of both, the host genome 48 and the acquired gene.  49  50 Methylobacterium mutations allow the adaptation to the presence of a foreign gene. 51  52 Some natural strains of Methylobacterium extorquens harbor a dehalogenase 53 dcmA gene, which has probably been acquired through horizontal gene transfer 54 4  (Vuilleumier et al. 2009). This gene is essential for the catabolism of Dichloromethane 55 and consequently for the growth of the bacteria in the presence of this toxic compound. 56 Using an in vitro evolution approach, Michener et al. (2014) have recently provided 57 suggestions of how this gene becomes a part of the M. extorquens genome. 58   Transformation with dcmA of different Methylobacterium species and M. 59 extorquens strains lacking the gene results initially in the minor growth of transformants 60 (compared to the wild strains of M. extorquens containing the gene) in presence of 61 Dichloromethane. However, after 150 generations of in vitro evolution in presence of 62 this compound, transformant strains with better fitness that the original strain appear. 63 Genome sequencing of these evolved strains have enabled authors to identify 64 regulatory mutations in four genes that appear to be associated to the improved fitness 65 of these strains. Some of these mutations affect genes involved in the chloride ions (a 66 byproduct of the metabolism of Dichloromethane) efflux to the extracellular medium, 67 which may explain the observed fitness increase. 68 Furthermore, the sequencing of the S. extorquens natural strains containing the 69 dcmA gene have revealed mutations on the clcA (one of the genes identified in evolved 70 strains which encodes an antiporter protein associated to chloride efflux) promoter that 71 improve gene expression as compared to strains lacking the dcmA gene. 72 What this study shows is how important is the recipient genetic background to 73 ensure the stable integration of an acquired gene. The evolution of the recipient genome 74 post-gene transfer, or the presence of a receptor possessing a permissive genetic 75 background, may allow the exploitation of the potential advantages that the acquisition 76 of a new (although initially harmful) gene can provides 77 . 78  79 5  Sequential horizontal transfer in Pseudomonas allows the stabilization of 80 horizontally acquired nitrogenase genes. 81  82 In the wild some Pseudomonas strains have acquired horizontally nitrogenase 83 genes that enable bacteria to fix nitrogen. However in the laboratory, the transformation 84 of Pseudomonas strains with nitrogenase genes results in phenotypes that reveal the 85 constitutive expression of the acquired genes (Setten et al. 2013) suggesting that 86 acquisition of these genes may initially be harmful to recipient. 87 A recent study by Pascuan et al. (2015) suggest the way by which nitrogenase 88 genes may have become a part of Pseudomonas genomes. In this study, the authors 89 identify horizontally acquired genes involved in the biosynthesis of Polyhydroxibutyrate 90 (PHB) in strains of Pseudomonas that fix nitrogen naturally. Next, authors transform 91 recombinant strains of Pseudomonas protegens harboring nitrogenase genes with the 92 PHB biosynthesis genes. Results clearly show that the presence of PHB genes 93 contributes to the regulation of the expression of nitrogenase, suggesting that the 94 presence of PHB genes in the receptor alleviate the problems caused by the presence of 95 nitrogenase genes. 96 In this case, sequential horizontal gene transfer seems to be an important 97 contributor towards the stable integration of the acquired genes. As in the case of 98 Methylobacterium, the evolution of the recipient genome through the acquisition of new 99 genes or the transfer to a recipient that has previously acquired permissive genes leads 100 to the stable acquisition of an initially detrimental gene. In this way, it is possible to 101 exploit the advantages that the new gene may provide. 102  103 Post-transfer gene modifications allow the stable integration of foreign genes. 104 6   105  Several studies have shown the importance of amelioration of horizontally 106 acquired genes for their stable and long term maintenance in the recipient organism 107 (Marri and Golding 2008).Over time, changes in codon usage and base composition 108 improve the transcription and translation of the acquired gene in the new host.  109 In a very recent paper Llorente et al. (2016) go one step ahead, underlining the 110 role of the acquisition of new sequences that enable the correct cellular targeting of the 111 gene product in the host cell. In this paper, the authors identify in plants a genomic gene 112 acquired from bacteria which are different from the cyanobacteria precursors of 113 chloroplasts. This gene encodes a plastid Polyphenol oxidase (PPO) and contains plastid 114 targeting signals that allow the gene product to travel from the nucleus to the 115 chloroplast. 116   Using a genetic engineering approach, the authors show that the deletion of the 117 targeting signals leads to the cytosolic localization of the gene product and that the 118 cytosolic localization of the enzyme reduces the plant growth. In this way, authors 119 conclude that the acquisition of targeting signals after the horizontal gene transfer is 120 necessary for the stabilization of the acquired gene. 121  122 To conclude, these three studies give us important new keys to understand how 123 foreign genes become successfully integrated in a new host, and how this integration 124 provides the recipient organism with novel options to exploit new habitats and 125 resources. 126  127  128  129 7   130 References 131  132  Baltrus DA. (2013) Exploring the costs of horizontal gene transfer. Trends Ecol. Evol. 133 28:489-495 134 Boto L (2015) Evolutionary change and phylogenetic relationships in light of horizontal 135 gene transfer. J. Biosc. 40:465-472 136 Llorente B, De Souza FSJ, Soto G, Meyer C, Alonso GD, Flawiá MM, Bravo-137 Almonacid F, Ayub ND, Rodriguez-Concepción M (2016) Selective pressure against 138 horizontally acquired prokaryotic genes as a driving force of plastid evolution. Sci. 139 Reports 6:19036 140 Marri PR, Golding GB (2008) Gene amelioration demonstrated: the journey of nascent 141 genes in bacteria. Genome 51:164-168 142 Michener JK,  Camargo Neves AA, Vuilleumier  S, Bringel F,  Marx CJ (2014) 143 Effective use of a horizontally-transferred pathway for dichloromethane catabolism 144 requires post-transfer refinement. Elife 3:e04279 145  Pascuan C, Fox AR, Soto G, Ayub ND (2015) Exploring the ancestral mechanisms of 146 regulation of horizontally acquired nitrogenases. J. Mol. Evol. 81:84-89 147 Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene 148 transfer between bacteria. Nat. Rev. Microbiol. 3:711-721 149 Setten L, Soto G, Mozzicafreddo M, Romina Fox A, Lisi C, Cuccioloni M, Angeletti M, 150 Pagano E, Diaz-Paleo A, Ayub, ND (2013) Engineering Pseudomonas protegens Pf-5 151 for nitrogen fixation and its application to improve plant growth under nitrogen-152 deficient conditions. Plos One 8:e63666 153 8  Vuilleumier S, Chistoserdova L, Lee MC, Bringel F, Lajus A, Zhou Y, Gourion B, 154 Barbe V, Chang J, Cruveiller S, Dossat C, Gillett W, Gruffaz C, Haugen E, Hourcade E, 155 Levy R, Mangenot S, Muller E, Nadalig T, Pagni M, Penny C, Peyraud R, Robinson 156 DG, Roche D, Rouy Z, Saenampechek C, Salvignol G, Vallenet D, Wu Z, Marx, CJ, 157 Vorholt JA, Olson MV, Kaul R, Weissenbach J, Medigue C, Lidstrom ME 158  (2009) Methylobacterium genome sequences: A reference blueprint to investigate 159 microbial metabolism of C1 compounds from natural and industrial sources. Plos One 160 4:e5584 161  162  163 

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