The phytopathogenic nature of Dickeya aquatica 174/2 and the dynamic early evolution of Dickeya pathogenicity

Abstract

Originality-Significance statementAlthough the reach of large-scale comparative studies has spread exponentially over the years, the phytopathogenic Dickeya group remains overlooked. In this work, we sequence the complete genome of Dickeya aquatica type strain, a species isolated from water that was first assumed to be non-phytopathogenic. We show that the proteome of D. aquatica contains a wide number of proteins involved in Dickeya virulence, including plant cell wall degrading enzymes, suggesting that this species could be in fact pathogenic. Using experimental approaches, we confirm this prediction and uncover the particular affinity of D. aquatica for acidic fruits. In-depth phylogenomic analyses reveal that Dickeya species display a great degree of genetic plasticity in the pathogenicity determinants, explaining how this bacterial group was able to colonize a wide variety of plants growing in different climates. These observations greatly advance our understanding of how bacteria adapt to new ecological niches.\n\nSummaryDickeya is a genus of phytopathogenic enterobacterales causing soft rot in a variety of plants (e.g. potato, chicory, maize). Among the species affiliated to this genus, Dickeya aquatica, described in 2014, remained particularly mysterious because it had no known host. Furthermore, while D. aquatica was proposed to represent a deep-branching species among Dickeya genus, its precise phylogenetic position remained elusive.\n\nHere, we report the complete genome sequence of the D. aquatica type strain 174/2. We demonstrate the affinity of D. aquaticaT for acidic fruits such as tomato and cucumber, and show that exposure of this bacterium to acidic pH induces twitching motility. An in-depth phylogenomic analysis of all available Dickeya proteomes pinpoints D. aquatica as the second deepest branching lineage within this genus and reclassifies two lineages that likely correspond to new genomospecies (gs.): Dickeya gs. poaceaephila (Dickeya sp NCPPB 569) and Dickeya gs. undicola (Dickeya sp 2B12), together with a new putative genus, tentatively named Prodigiosinella. Finally, from comparative analyses of Dickeya proteomes we infer the complex evolutionary history of this genus, paving the way to study the adaptive patterns and processes of Dickeya to different environmental niches and hosts. In particular, we hypothetize that the lack of xylanases and xylose degradation pathways in D. aquatica could reflects adaptation to aquatic charophyte hosts which, in contrast to land plants, do not contain xyloglucans.