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Phylogenomic fingerprinting of tempo and functions of horizontal gene transfer within ochrophytes

Richard G Dorrell, Adrien Villain, Benoît Perez-Lamarque [...] Hélène Morlon, Chris Bowler, Guillaume Blanc

Richard G Dorrell*, Adrien Villain, Benoît Perez-Lamarque, Guillemette Audren de Kerdrel, Giselle McCallum, Andrew K Watson, Ouardia Ait-Mohamed, Adriana Alberti, Erwann Corre, Kyle R Frischkorn, Juan J Pierella Karlusich, Eric Pelletier, Hélène Morlon, Chris Bowler, Guillaume Blanc*.


Horizontal gene transfer (HGT) is an important source of novelty in eukaryotic genomes. This is particularly true for the ochrophytes, a diverse and important group of algae. Previous studies have shown that ochrophytes possess a mosaic of genes derived from bacteria and eukaryotic algae, acquired through chloroplast endosymbiosis and from HGTs, although understanding of the time points and mechanisms underpinning these transfers has been restricted by the depth of taxonomic sampling possible. We harness an expanded set of ochrophyte sequence libraries, alongside automated and manual phylogenetic annotation, in silico modeling, and experimental techniques, to assess the frequency and functions of HGT across this lineage. Through manual annotation of thousands of single-gene trees, we identify continuous bacterial HGT as the predominant source of recently arrived genes in the model diatom Phaeodactylum tricornutum Using a large-scale automated dataset, a multigene ochrophyte reference tree, and mathematical reconciliation of gene trees, we note a probable elevation of bacterial HGTs at foundational points in diatom evolution, following their divergence from other ochrophytes. Finally, we demonstrate that throughout ochrophyte evolutionary history, bacterial HGTs have been enriched in genes encoding secreted proteins. Our study provides insights into the sources and frequency of HGTs, and functional contributions that HGT has made to algal evolution.
Keywords : MMETSP ; RNAseq ; ornithine-urea cycle ; phylogenomics ; stramenopile.

* Correspondence should be addressed to Richard Dorrell and Guillaume Blanc

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This project was carried out in collaboration between the teams of Chris Bowler (R.G.D, G.A.d.K., G.M., O.A.M., J.J.P.K., K.R.F., C.B.) and Hélène Morlon (B.P-L., H.M.).
The authors thank the Ecole Normale Supérieure for support of the research of B. P-L. (doctoral student) and G.A.d.K. (L3 summer student).

Proc Natl Acad Sci USA. 2021 Jan 26 ; 118(4) : e2009974118. doi : 10.1073/pnas.2009974118