Comprehensive and Functional Analysis of Horizontal Gene Transfer Events in Diatoms

Abstract

Diatoms are a diverse group of mainly photosynthetic algae, responsible for 20% of worldwide oxygen production, which can rapidly respond to favourable conditions and often outcompete other phytoplankton. We investigated the contribution of horizontal gene transfer (HGT) to its ecological success. A large-scale phylogeny-based prokaryotic HGT detection procedure across nine sequenced diatoms showed that 3-5% of their proteome has a horizontal origin and a large influx occurred at the ancestor of diatoms. More than 90% of HGT genes are expressed, and species-specific HGT genes in Phaeodactylum tricornutum undergo strong purifying selection. Genes derived from HGT are implicated in several processes including environmental sensing, and expand the metabolic toolbox. Cobalamin (vitamin B12) is an essential cofactor for roughly half of the diatoms and is only produced by bacteria. Five consecutive genes involved in the final synthesis of the cobalamin biosynthetic pathway, which could function as scavenging and repair genes, were detected as HGT. The full suite of these genes were detected in the cold-adapted diatom Fragilariopsis cylindrus. This might give diatoms originating from the Southern Ocean, a region typically depleted in cobalamin, a competitive advantage. Overall, we show that HGT is a prevalent mechanism that is actively used in diatoms to expand its adaptive capabilities.

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

“…2 and 3). Our data underscore how HGTs from a range of different sources have impacted on the evolution of eukaryotic micro-organisms, a concept that has been the subject of extensive debate (56)(57)(58). Further phylogenetic reconstructions, using denser taxonomic sampling strategies may detect even greater numbers of HGTs in P. tricornutum.…”

Re-examination of two diatom reference genomes using long-read sequencing

“…A total of 7512 (45.6%) T. pseudonana genes predicted in our study were assigned to these groups; 5136 genes were inferred to be diatom-specific, 1959 as shared with other stramenopile lineages (e.g., oomycetes, Blastocystidae, Pelagophyceae) and 1082 as having strong similarity to bacteria (predominantly Proteobacteria) as determined by subsequent PLAST analyses against the NCBI protein database. The T. pseudonana genes with a strong affinity to bacteria were not investigated further, although they could represent instances of HGT, as inferred by previous studies [11,13].…”

“…The original T. pseudonana and P. tricornutum genome projects also shed light on the complex evolutionary history of diatoms. Both diatom genomes were found to be a mosaic of both heterotrophic host and algal endosymbiont genes, as well as apparently non-endosymbiotic, bacterial genes predicted to have been acquired via horizontal gene transfer (HGT) [ 3 , 11 – 13 ]. Previous diatom genomic studies also demonstrated that transposable elements (TEs) are present in both genomes but are more prominent in P. tricornutum (8.4% of the P. tricornutum genome [ 14 ] vs. 1.9% in T. pseudonana [ 15 ]).…”

“…The original T. pseudonana and P. tricornutum genome projects also shed light on the complex evolutionary history of diatoms. Both diatom genomes were found to be a mosaic of both heterotrophic host and algal endosymbiont genes, as well as apparently nonendosymbiotic, bacterial genes predicted to have been acquired via horizontal gene transfer (HGT) [3,[11][12][13].…”

Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida

“…Recent studies estimated that 3-5% of genes in diatom genomes were acquired through species-specific horizontal gene transfer (HGT) (Vancaester et al 2020). For N. putrida, we identified 73 genes potentially acquired via HGT based on phylogenetic tree reconstruction.…”