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

doi:10.1016/j.cell.2022.12.006

Novel integrative elements and genomic plasticity in ocean ecosystems

Cell. 2023 Jan 5;186(1):47-62.e16. doi: 10.1016/j.cell.2022.12.006.

Authors

Thomas Hackl¹, Raphaël Laurenceau², Markus J Ankenbrand³, Christina Bliem², Zev Cariani², Elaina Thomas², Keven D Dooley², Aldo A Arellano², Shane L Hogle², Paul Berube², Gabriel E Leventhal², Elaine Luo⁴, John M Eppley⁴, Ahmed A Zayed⁵, John Beaulaurier⁶, Ramunas Stepanauskas⁷, Matthew B Sullivan⁸, Edward F DeLong⁴, Steven J Biller⁹, Sallie W Chisholm¹⁰

Affiliations

¹ Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA 02139, USA; Groningen Institute for Evolutionary Life Sciences, University of Groningen, 9700CC Groningen, the Netherlands. Electronic address: t.hackl@rug.nl.
² Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA 02139, USA.
³ Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA 02139, USA; University of Würzburg, Center for Computational and Theoretical Biology, 97070 Würzburg, Germany.
⁴ Daniel K. Inouye Center for Microbial Oceanography, Research and Education, University of Hawai'i Manoa, Honolulu, HI 96822, USA.
⁵ EMERGE Biology Integration Institute, Ohio State University, Columbus, OH 43210, USA; Center of Microbiome Science, Ohio State University, Columbus, OH 43210, USA.
⁶ Oxford Nanopore Technologies Inc, San Francisco, CA 94501, USA.
⁷ Bigelow Laboratory for Ocean Sciences, East Boothbay, ME 04544, USA.
⁸ Department of Microbiology & Department of Civil, Environmental, and Geodetic Engineering, Ohio State University, Columbus, OH 43210, USA; EMERGE Biology Integration Institute, Ohio State University, Columbus, OH 43210, USA; Center of Microbiome Science, Ohio State University, Columbus, OH 43210, USA.
⁹ Wellesley College, Department of Biological Sciences, Wellesley, MA 02481, USA.
¹⁰ Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA 02139, USA; Massachusetts Institute of Technology, Department of Biology, Cambridge, MA 02139, USA. Electronic address: chisholm@mit.edu.

PMID: 36608657
DOI: 10.1016/j.cell.2022.12.006

Abstract

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.

Keywords: Prochlorococcus; adaptation; extracellular vesicles; genomic islands; horizontal gene transfer; mobile genetic elements; pangenome; viral satellites.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Ecosystem*
Genome, Bacterial* / genetics
Genomics
Oceans and Seas
Phylogeny