Role of Integrative Elements in Gene Transfer and Niche Adaptation in Prochlorococcus

Elaina Thomas1, Thomas Hackl1, Raphaël Laurenceau1, Markus J Ankenbrand1,2, Christina Bliem1, Zev Cariani1, Paul Berube1, Steven Biller1, Ramunas Stepanauskas3 and Sallie W Chisholm1,4, (1)Massachusetts Institute of Technology, Civil and Environmental Engineering, Cambridge, MA, United States, (2)University Hospital Würzburg, Comprehensive Heart Failure Center, Würzburg, Germany, (3)Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, United States, (4)Massachusetts Institute of Technology, Biology, Cambridge, MA, United States
Abstract:
The marine cyanobacterium Prochlorococcus is globally abundant and ecologically diverse. While each cell has a small, streamlined genome, the Prochlorococcus ‘collective’ displays remarkable genome flexibility and possesses an extensive pangenome, suggesting frequent genetic exchange. Conjugation and transformation – common modes of horizontal gene transfer – appear to be absent in Prochlorococcus, suggesting these cells may employ another system of gene exchange.

We show that Prochlorococcus genomes contain a previously unknown type of mobile genetic element. These elements are located within genomic islands, which are hotspots for flexible genes, i.e. genes not shared by all Prochlorococcus. The majority of the elements use tRNAs within islands as integration sites. To examine element regulation, Prochlorococcus cultures were subjected to mitomycin C-induced DNA damage. This resulted in upregulation of integration, excision, and replication genes within elements. Based on this and the similarity of some of the elements to phage-inducible sequences, the elements appear to be tightly regulated and induced by intense stress, such as phage infection. It appears the elements can be transmitted via vesicles as they are enriched in extracellular vesicle metagenomes. The elements vary in gene content and contain ecologically relevant cargo, including operons for nutrient acquisition and phage defense.

Vesicle-mediated transfer of the elements could explain the diversification of Prochlorococcus across wide-ranging environments, and could elucidate the ways in which the Prochlorococcus ‘collective’ maintains a flexible, extensive pangenome while the genomes of individual cells are streamlined. Considering the global abundance of Prochlorococcus and the possibility this system functions in other streamlined free-living oceanic microbes, this mode of gene transfer has the potential to transform our understanding of microbial evolution and diversification in marine ecosystems.

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