The genomic signature of viral predation in free living bacteria

Background/Question/Methods

Globally ubiquitous and abundant bacteria have the smallest genomes of known free-living microorganisms. The prevailing explanation for this observation is genome “streamlining” to reduce elemental costs of growth thus increasing their competitiveness which could lead to their observed dominance. However, there appears to be no relationship between genome size and fitness related characteristics such as growth rate. An alternative explanation is abundant bacteria achieve numerical dominance by avoiding viruses through cell size minimization, slow growth rates, and deletion of genes coding for cell surface structures that are targeted by viruses. There is mounting evidence indicating that abundant bacteria are targeted by profuse and diverse array of viruses, grow very slowly, are neither motile nor chemotactic, and have small cell sizes. All these characteristics suggest virus avoidance is an important part of abundant species ecology. We hypothesize that reduction in genome size is accompanied by disproportionate decrease in virus targets such as surface localized proteins or flagella. To investigate this we interrogated genomes of free living organisms available in current databases. We compared genome size to proportion of genes localized to cell surfaces, and presence or absence of known virus targets including flagella, fimbriae, and histidine kinases.

Results/Conclusions

Based on the genomes of over 800 free living bacteria we found a statistically significant negative relationship between genome size and proportion of surface localized proteins. Additionally, genomes from known globally abundant bacteria have proportionally less surface proteins than the average (all greater than one standard deviation below the mean of all bacteria). Bacteria with small genomes also appear to be less likely to have flagella or fimbriae. These observations support the hypothesis that genome reduction is driven by pressure to minimize virus targets. Furthermore, we know that abundance elevates predation risk (Kill-The-Winner hypothesis) and these results suggest bacteria may achieve numerical dominance by minimizing other factors of predation risk. The apparent cost of this strategy is slow growth, minimal metabolic flexibility, and a passive minimalist lifestyle.