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Novel integrative elements and genomic plasticity in ocean ecosystems

View ORCID ProfileThomas Hackl, View ORCID ProfileRaphaël Laurenceau, View ORCID ProfileMarkus J. Ankenbrand, View ORCID ProfileChristina Bliem, Zev Cariani, View ORCID ProfileElaina Thomas, View ORCID ProfileKeven D. Dooley, View ORCID ProfileAldo A. Arellano, View ORCID ProfileShane L. Hogle, View ORCID ProfilePaul Berube, View ORCID ProfileGabriel E. Leventhal, View ORCID ProfileElaine Luo, View ORCID ProfileJohn Eppley, View ORCID ProfileAhmed A. Zayed, View ORCID ProfileJohn Beaulaurier, View ORCID ProfileRamunas Stepanauskas, View ORCID ProfileMatthew B. Sullivan, View ORCID ProfileEdward F. DeLong, View ORCID ProfileSteven J. Biller, View ORCID ProfileSallie W. Chisholm
doi: https://doi.org/10.1101/2020.12.28.424599
Thomas Hackl
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
2Max Planck Institute for Medical Research, Biomolecular Mechanisms, Heidelberg, Germany
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  • For correspondence: thackl@mit.edu chisholm@mit.edu
Raphaël Laurenceau
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Markus J. Ankenbrand
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
3University of Würzburg, Center for Computational and Theoretical Biology, Würzburg, Germany
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Christina Bliem
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Zev Cariani
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Elaina Thomas
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Keven D. Dooley
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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  • ORCID record for Keven D. Dooley
Aldo A. Arellano
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Shane L. Hogle
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Paul Berube
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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Gabriel E. Leventhal
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
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  • ORCID record for Gabriel E. Leventhal
Elaine Luo
4Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i Manoa, Honolulu, HI, USA
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John Eppley
4Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i Manoa, Honolulu, HI, USA
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Ahmed A. Zayed
6EMERGE Biology Integration Institute, Ohio State University, Columbus, OH, USA
7Center of Microbiome Science, Ohio State University, Columbus, OH, USA
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John Beaulaurier
8Oxford Nanopore Technologies Inc., San Francisco, CA, USA
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Ramunas Stepanauskas
9Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA
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Matthew B. Sullivan
5Department of Microbiology & Department of Civil, Environmental, and Geodetic Engineering, Ohio State University, Columbus, OH, USA
6EMERGE Biology Integration Institute, Ohio State University, Columbus, OH, USA
7Center of Microbiome Science, Ohio State University, Columbus, OH, USA
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Edward F. DeLong
4Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawai’i Manoa, Honolulu, HI, USA
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Steven J. Biller
10Wellesley College, Department of Biological Sciences, Wellesley, MA, USA
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Sallie W. Chisholm
1Massachusetts Institute of Technology, Department of Civil and Environmental Engineering, Cambridge, MA, USA
11Massachusetts Institute of Technology, Department of Biology, Cambridge, MA, USA
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  • For correspondence: thackl@mit.edu chisholm@mit.edu
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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.

Competing Interest Statement

JB is an employee of Oxford Nanopore Technologies and is a shareholder and/or share option holder.

Footnotes

  • https://doi.org/10.5281/zenodo.4393629

  • https://github.com/thackl/pro-tycheposons

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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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 Eppley, Ahmed A. Zayed, John Beaulaurier, Ramunas Stepanauskas, Matthew B. Sullivan, Edward F. DeLong, Steven J. Biller, Sallie W. Chisholm
bioRxiv 2020.12.28.424599; doi: https://doi.org/10.1101/2020.12.28.424599
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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 Eppley, Ahmed A. Zayed, John Beaulaurier, Ramunas Stepanauskas, Matthew B. Sullivan, Edward F. DeLong, Steven J. Biller, Sallie W. Chisholm
bioRxiv 2020.12.28.424599; doi: https://doi.org/10.1101/2020.12.28.424599

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