Novel integrative elements and genomic plasticity in ocean ecosystems

• DOI: 10.1016/j.cell.2022.12.006
• Publication Date: 2023-01-05T15:39:31Z
• Authors: Thomas Hackl; Raphaël Laurenceau; Markus J. Ankenbrand; Christina Bliem; Zev Cariani; Elaina Thomas; Keven D. Dooley; Aldo A. Arellano; Shane L. Hogle; Paul Berube; Gabriel E. Leventhal; Elaine Luo; John M. Eppley; Ahmed A. Zayed; John Beaulaurier; Ramunas Stepanauskas; Matthew B. Sullivan; Edward F. DeLong; Steven J. Biller; Sallie W. Chisholm
• Keywords: 0301 basic medicine; 0303 health sciences; pangenome; Oceans and Seas; mobile genetic elements; adaptation; Genomics; viral satellites; genomic islands; 03 medical and health sciences; 13. Climate action; horizontal gene transfer; 14. Life underwater; extracellular vesicles; Ecosystem; Genome, Bacterial; Phylogeny; Prochlorococcus

Horizontal gene transfer accelerates microbial evolution, promoting diversification and adaptation. The globally abundant marine cyanobacteriumProchlorococcushas a highly streamlined genome with frequent gene exchange reflected in its extensive pangenome. The source of its genomic variability, however, remains elusive since most cells lack the common mechanisms that enable horizontal gene transfer, including conjugation, transformation, plasmids and prophages. Examining 623 genomes, we reveal a diverse system of mobile genetic elements – cargo-carrying transposons we named tycheposons – that shapeProchlorococcus’ genomic plasticity. The excision and integration of tycheposons at seven tRNA genes drive the remodeling of larger genomic islands containing most ofProchlorococcus’ flexible genes. Most tycheposons carry genes important for niche differentiation through nutrient acquisition; others appear similar to phage parasites. Tycheposons are highly enriched in extracellular vesicles and phage particles in ocean samples, suggesting efficient routes for their dispersal, transmission and propagation. Supported by evidence for similar elements in other marine microbes, our work underpins the role of vesicle- and virus-mediated transfer of mobile genetic elements in the diversification and adaptation of microbes in dilute aquatic environments – adding a significant piece to the puzzle of what governs microbial evolution in the planet’s largest habitat.