Genomic island variability facilitates Prochlorococcus-virus coexistence

Both Prochlorococcus and the viruses that infect them are ubiquitous in the marine environment. The underlying mechanisms that allows the coexistence of Prochlorococcus and viruses in nature remains unclear. However, one such hypotheses that have been put forward to explain this phenomena is the continuous arms race between Prochlorococcus and strain-specific viruses. In this paper, they combined whole-genome sequencing and PCR techniques to investigate the effect of resistance on genome evolution and the genomic mechanisms behind the long-term coexistence.

The experiment studied the genome of 77 substrains that is selected for resistance to 10 podoviruses. The substrains used are from two different ecotype which differs in their geographic distribution. These substrains have shown majority of mutations in the hypervariable genomic island, with 71% localised to a single genomic island, ISL4, indicating that this is a virus susceptible region. The mutations affects viral attachment to the cell surface and imposed a fitness cost by decreasing growth rate to the host. This identification of resistance-conferring mutations in the genes suggest that the genomic islands are dynamic and genomic mutation occurs not by chance but rather are directly associated with viral selection pressure.  

Mutation confer resistance to specific phages might be seen as favourable to the survival of Prochlorococcus, but the authors have shown that it allow more rapid infection by other phages. Which is termed as “enhanced infection dynamics” fitness cost. In this study, they have shown that at least 16 out of the 23 mutant substrains studied have showed adaptive cost resistance- which is either reduced growth rate of more rapid infection by other viruses.

To test for the coexistence of cyanobacteria-virus, their findings suggest that resistant Prochlorococcus population probably exist in the environment and is highly diverse. The experiments have shown high rate of mutation which leads to resistance in the substrain MED4. This spontaneous mutation is 10-1000 fold higher than other bacteria.

It is well accepted that gene acquisition is facilitated by horizontal gene transfer mediated both by phages and by other mobile genetic elements, and that the genomic islands are a repository for such horizontally acquired genes. Horizontal gene transferred in genomic islands is beneficial to microbes as it facilitates constant gene flow and generates numerous polymorphisms which effectively reduce the population size for infection by any particular phage.   

The authors proposed that the “arms race” between bacteria and their viruses leads to the emergence of resistant bacteria in both a sequential and accumulative process, resulting in a continuum of cyanobacteria with different but overlapping ranges of viral susceptibility. This also further brings in the “numerical refuge hypothesis”. This study have thus evidence 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. 

Avrani, S., Wurtzel, O., Sharon, I., Sorek, R. and Lindell, D. (2011) Genomic island variability facilitates Prochlorococcus–virus coexistence. Nature. 474, 606-608.