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Genomic island variability facilitates Prochlorococcus–virus coexistence

Nature volume 474, pages 604–608 (2011)Cite this article

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Abstract

Prochlorococcus cyanobacteria are extremely abundant in the oceans, as are the viruses that infect them. How hosts and viruses coexist in nature remains unclear, although the presence of both susceptible and resistant cells may allow this coexistence. Combined whole-genome sequencing and PCR screening technology now enables us to investigate the effect of resistance on genome evolution and the genomic mechanisms behind the long-term coexistence of Prochlorococcus and their viruses. Here we present a genome analysis of 77 substrains selected for resistance to ten viruses, revealing mutations primarily in non-conserved, horizontally transferred genes that localize to a single hypervariable genomic island. Mutations affected viral attachment to the cell surface and imposed a fitness cost to the host, manifested by significantly lower growth rates or a previously unknown mechanism of more rapid infection by other viruses. The mutant genes are generally uncommon in nature yet some carry polymorphisms matching those found experimentally. These data are empirical evidence indicating that viral-attachment genes are preferentially located in genomic islands and that viruses are a selective pressure enhancing the diversity of both island genes and island gene content. This diversity emerges as a genomic mechanism that reduces the effective host population size for infection by a given virus, thus facilitating long-term coexistence between viruses and their hosts in nature.

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Figure 1: Distribution of resistance-conferring mutations.
Figure 2: Phylogeny of representative MED4 mutant genes.
Figure 3: Attachment of podoviruses to resistant substrains.
Figure 4: Cost of resistance.
Figure 5: Resistance-conferring genes in the environment.

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Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The DNA polymerase and g20 sequences of the phages isolated in this study have been submitted to Genbank under the accession numbers JF837212 to JF837216.

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Acknowledgements

We thank E. Zinser for the bacterial helper strain; I. Pekarsky for help with adsorption assays; I. Izhaki for advice on statistical analyses; O. Beja, Y. Mandel-Gutfreund, K. Kozek, U. Qimron and Lindell lab members for comments on the manuscript; and T. Dagan for coining the term ‘susceptibility region’. Genome sequencing was carried out at the genome sequencing units at the Weizmann Institute of Science and the Technion – Israel Institute of Technology. This work was supported by a European Commission ERC Starting Grant (no. 203406), an ISF Morasha grant (no. 1504/06) and the Technion Russell Berrie Nanotechnology Institute (D.L.); and by an ISF-FIRST grant (no. 1615/09) and an ERC Starting Grant (R.S.). O.W. was supported by an Azrieli fellowship and D.L. is a Shillman fellow.

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Author notes

  1. Itai Sharon

    Present address: Present address: Department of Earth and Planetary Science, University of California, Berkeley, California 94720, USA.,

Authors and Affiliations

  1. Faculty of Biology, Technion – Israel Institute of Technology, Haifa 32000, Israel

    Sarit Avrani, Itai Sharon & Debbie Lindell

  2. Department of Molecular Genetics, Weizmann Institute of Science, Rehovot 76100, Israel

    Omri Wurtzel & Rotem Sorek

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  1. Sarit Avrani
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Contributions

S.A. and D.L. designed the project and the experiments; S.A. performed and analysed the laboratory experiments, PCR screening and phylogenetic analyses; O.W. performed the bioinformatic analyses and, together with R.S., analysed the genome sequencing data; I.S. analysed the environmental sequences; and D.L. wrote the manuscript with significant contributions from all authors.

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Correspondence to Debbie Lindell.

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The authors declare no competing financial interests.

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The file contains Supplementary Methods, Supplementary References, Supplementary Tables 1-7 and Supplementary Figures 1-8 with legends. (PDF 1647 kb)

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Avrani, S., Wurtzel, O., Sharon, I. et al. Genomic island variability facilitates Prochlorococcus–virus coexistence. Nature 474, 604–608 (2011). https://doi.org/10.1038/nature10172

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