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Abstract Lateral gene transfer is a major evolutionary process in Bacteria and Archaea. Despite its importance, lateral gene transfer quantification in nature using traditional phylogenetic methods has been hampered by the rarity of most genes within the enormous microbial pangenomes. Here, we estimated lateral gene transfer rates within the epipelagic tropical and subtropical ocean using a global, randomized collection of single amplified genomes and a non-phylogenetic computational approach. By comparing the fraction of shared genes between pairs of genomes against a lateral gene transfer-free model, we show that an average cell line laterally acquires and retains ~13% of its genes every 1 million years. This translates to a net lateral gene transfer rate of ~250 genes L−1 seawater day−1 and involves both “flexible” and “core” genes. Our study indicates that whereas most genes are exchanged among closely related cells, the range of lateral gene transfer exceeds the contemporary definition of bacterial species, thus providing prokaryoplankton with extensive genetic resources for lateral gene transfer-based adaptation to environmental stressors. This offers an important starting point for the quantitative analysis of lateral gene transfer in natural settings and its incorporation into evolutionary and ecosystem studies and modeling. 

Abstract Several species of sacoglossan sea slugs possess the incredible ability to sequester chloroplasts from the algae they consume. These “photosynthetic animals” incorporate stolen chloroplasts, called kleptoplasts, into the epithelial cells of tubules that extend from their digestive tracts throughout their bodies. The mechanism by which these slugs maintain functioning kleptoplasts in the absence of an algal nuclear genome is unknown. Here, we report a draft genome of the sacoglossan slug Elysia crispata morphotype clarki, a morphotype native to the Florida Keys that can retain photosynthetically active kleptoplasts for several months without feeding. We used a combination of Oxford Nanopore Technologies long reads and Illumina short reads to produce a 786-Mb assembly (N50 = 0.459 Mb) containing 68,514 predicted protein-coding genes. A phylogenetic analysis found no evidence of horizontal acquisition of genes from algae. We performed gene family and gene expression analyses to identify E. crispata genes unique to kleptoplast-containing slugs that were more highly expressed in fed versus unfed developmental life stages. Consistent with analyses in other kleptoplastic slugs, our investigation suggests that genes encoding lectin carbohydrate-binding proteins and those involved in regulation of reactive oxygen species and immunity may play a role in kleptoplast retention. Lastly, we identified four polyketide synthase genes that could potentially encode proteins producing UV- and oxidation-blocking compounds in slug cell membranes. The genome of E. crispata is a quality resource that provides potential targets for functional analyses and enables further investigation into the evolution and mechanisms of kleptoplasty in animals.