Convergent evolution toward an improved growth rate and a reduced resistance range inProchlorococcusstrains resistant to phage

Abstract

Prochlorococcus is an abundant marine cyanobacterium that grows rapidly in the environment and contributes significantly to global primary production. This cyanobacterium coexists with many cyanophages in the oceans, likely aided by resistance to numerous co-occurring phages. Spontaneous resistance occurs frequently in Prochlorococcus and is often accompanied by a pleiotropic fitness cost manifested as either a reduced growth rate or enhanced infection by other phages. Here, we assessed the fate of a number of phage-resistant Prochlorococcus strains, focusing on those with a high fitness cost. We found that phage-resistant strains continued evolving toward an improved growth rate and a narrower resistance range, resulting in lineages with phenotypes intermediate between those of ancestral susceptible wild-type and initial resistant substrains. Changes in growth rate and resistance range often occurred in independent events, leading to a decoupling of the selection pressures acting on these phenotypes. These changes were largely the result of additional, compensatory mutations in noncore genes located in genomic islands, although genetic reversions were also observed. Additionally, a mutator strain was identified. The similarity of the evolutionary pathway followed by multiple independent resistant cultures and clones suggests they undergo a predictable evolutionary pathway. This process serves to increase both genetic diversity and infection permutations in Prochlorococcus populations, further augmenting the complexity of the interaction network between Prochlorococcus and its phages in nature. Last, our findings provide an explanation for the apparent paradox of a multitude of resistant Prochlorococcus cells in nature that are growing close to their maximal intrinsic growth rates.cyanobacteria | cyanophage | resistance | Prochlorococcus | virus

Transcriptome dynamics of a broad host-range cyanophage and its hosts

“…Thus, expression of island genes during infection may have led to their utilization by phages over evolutionary time and their stable incorporation into phage genomes . Third, phages serve as an important selective pressure influencing diversity and content of cell-surface genes in genomic islands (Avrani et al, 2011;Avrani and Lindell, 2015), the products of which are utilized by phage for attachment and entry into the host. Combined, these findings highlight the central role of hypervariable genomic islands in cyanobacterial host-phage interactions, serving as a central axis for host response and defense against phage infection, as well as a hotspot for dynamic gene exchange that continually reshapes the genomes of both host and phage.…”

Cross‐protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities

“…These heterotrophs included strains isolated as contaminants of the Prochlorococcus cultures, such as the gammaproteobacterium Alteromonas sp. Subsequent reports from other research groups have confirmed that Prochlorococcus can be helped during growth in liquid (Sher et al, 2011) and semisolid (Avrani and Lindell, 2015) culture media by heterotrophic bacteria. Additionally, dilute lawns of Prochlorococcus are unable to grow on plates, unless rescued by patches of helper cells (Morris et al, 2008, and Fig.…”

Emerging Interaction Patterns in the Emiliania huxleyi-EhV System

“…When Avrani and colleagues [29] observed a similar response in viral resistant Prochlorococcus strains, they also found that the reduced growth rates increased after 7 months and that these strains reduced their resistance against the viruses [84]. The changes in growth rate and resistance occurred as independent events, indicating that the selection pressure on these phenotypes was decoupled.…”

“…As also tried in the current study, COR is often measured as reduction of growth rates in the resistant host [23,24,25,26,27], but other CORs, like altered susceptibility to other viruses and possibly also to some bacteria [85], have also been argued [29,84,86,87,88]. Trade-off might also emerge when strains with different resistance capacities are put under competition for a limited level of nutrients [30,33,89,90], and this is the logical follow up to our study.…”