A Phylogenetic Host-Range Index Reveals Ecological Constraints in Phage Specialisation and Virulence.

Phages are typically known for having a limited host range, targeting particular strains within a bacterial species, but accurately measuring their specificity remains challenging. Factors like the genetic diversity or population dynamics of host bacteria are often disregarded despite their potential influence on phage specialisation and virulence. This study focuses on the Ralstonia solanacearum species complex (RSSC), which comprises genetically diverse bacteria responsible for a major plant disease. It uses a diversified collection of RSSC phages to develop new host-range analysis methods and to test ecological and evolutionary hypotheses on phage host range. We introduce a new 'phylogenetic host-range index' that employs an ecological diversity index to account for the genetic diversity of bacterial hosts, allowing systematic classification of phages along a continuum between specialists and generalists. We propose and provide evidence that generalist phages are more likely to be represented in CRISPR-Cas immune system of bacteria than specialist phages. We explore the hypothesis that generalist phages might exhibit lower virulence than specialist ones due to potential evolutionary trade-offs between host-range breadth and virulence. Importantly, contrasted correlations between phage virulence and host range depend on the epidemiological context. A trade-off was confirmed in a context of low bacterial diversity, but not in a context of higher bacterial diversity, where no apparent costs were detected for phages adapted to a wide range of hosts. This study highlights the need for genetic analyses in phage host range and of investigating ecological trade-offs that could improve both fundamental phage knowledge and applications in biocontrol or therapy.