Novel integrative elements and genomic plasticity in ocean ecosystems

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*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

23 Citations (Scopus)
159 Downloads (Pure)

Abstract

Horizontal gene transfer accelerates microbial evolution, promoting diversification and adaptation. The globally abundant marine cyanobacterium Prochlorococcus has 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 shape Prochlorococcus’ genomic plasticity. The excision and integration of tycheposons at seven tRNA genes drive the remodeling of larger genomic islands containing most of Prochlorococcus’ 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.

Original languageEnglish
Pages (from-to)47-62.e16
JournalCell
Volume186
Issue number1
DOIs
Publication statusPublished - 5-Jan-2023

Keywords

  • adaptation
  • extracellular vesicles
  • genomic islands
  • horizontal gene transfer
  • mobile genetic elements
  • pangenome
  • Prochlorococcus
  • viral satellites

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