Novel integrative elements and genomic plasticity in ocean ecosystems

• Published in: Cell Vol. 186; no. 1; pp. 47 - 62.e16
• Main Authors: Hackl, Thomas, Laurenceau, Raphaël, Ankenbrand, Markus J., Bliem, Christina, Cariani, Zev, Thomas, Elaina, Dooley, Keven D., Arellano, Aldo A., Hogle, Shane L., Berube, Paul, Leventhal, Gabriel E., Luo, Elaine, Eppley, John M., Zayed, Ahmed A., Beaulaurier, John, Stepanauskas, Ramunas, Sullivan, Matthew B., DeLong, Edward F., Biller, Steven J., Chisholm, Sallie W.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 05-01-2023; Elsevier
• Subjects: adaptation; Ecosystem; extracellular vesicles; Genome, Bacterial - genetics; genomic islands; Genomics; horizontal gene transfer; mobile genetic elements; Oceans and Seas; pangenome; Phylogeny; Prochlorococcus; viral satellites; Prochlorococcus; pangenome; extracellular vesicles; genomic islands; mobile genetic elements; adaptation; viral satellites; horizontal gene transfer
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2022.12.006

Horizontal gene transfer accelerates microbial evolution. The marine picocyanobacterium Prochlorococcus exhibits high genomic plasticity, yet the underlying mechanisms are elusive. Here, we report a novel family of DNA transposons—“tycheposons”—some of which are viral satellites while others carry cargo, such as nutrient-acquisition genes, which shape the genetic variability in this globally abundant genus. Tycheposons share distinctive mobile-lifecycle-linked hallmark genes, including a deep-branching site-specific tyrosine recombinase. Their excision and integration at tRNA genes appear to drive the remodeling of genomic islands—key reservoirs for flexible genes in bacteria. In a selection experiment, tycheposons harboring a nitrate assimilation cassette were dynamically gained and lost, thereby promoting chromosomal rearrangements and host adaptation. Vesicles and phage particles harvested from seawater are enriched in tycheposons, providing a means for their dispersal in the wild. Similar elements are found in microbes co-occurring with Prochlorococcus, suggesting a common mechanism for microbial diversification in the vast oligotrophic oceans.
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•Tycheposons are novel DNA transposons promoting genomic adaptation in marine bacteria•Tycheposons can be viral satellites or carry cargo such as nutrient-acquisition genes•Tycheposons are abundant in viral capsids and extracellular vesicles in seawater•Tycheposons accelerate genomic island formation and remodeling
Tycheposons, a group of mobile genetic elements, facilitate horizontal gene transfer in marine picocyanobacteria. Dispersed through viral capsids and extracellular vesicles, tycheposons promote genomic diversification and adaptation, accelerating microbial evolution across our planet's largest habitat.