The role of actinobacteria in growth-promotion and metabolome modulation in Mediterranean plants: nature-based solutions for sustainable food production

Plant-derived bioactive compounds are abundant in Mediterranean species like oregano and tomato, offering valuable applications in human health-related fields. Microbial-based biostimulants (MBBs), particularly those rich in microbes from the phylum Actinomycetota (previously Actinobacteria), represent a promising approach to drive the transition of agricultural systems towards sustainable and better agroecological practices. In this study, two soil Actinomycetota - Streptomyces violaceoruber and Kocuria rhizophila, alone or in consortium - were assayed as Plant Growth-Promoting Bacteria (PGPB) on oregano and tomato plants under controlled laboratory conditions, greenhouse, and open field experiments that were carried out only for oregano. The aim was to assess their influence on plant growth and metabolite yield. S. violaceoruber and K. rhizophila positively influenced several morpho-physiological parameters of the investigated plants: inoculations improved germination rate, shoot heights, and chlorophyll content in oregano and shoot heights, leaf area and biomass yield in tomato. Both species exhibited significant changes in their metabolic profiles following PGPB inoculations. In particular, Gas Chromatography-Mass Spectrometry (GC-MS) analyses of oregano revealed a modulation in terpenes production, both in the flower volatilome and essential oils, while, in tomato, an increased proline content was detected. The different transcriptomic responses after the inoculations suggested a different involvement of the two Actinomycetota in the modulation of tomato biosynthetic pathways. In parallel, a collection of bacterial strains was isolated from the oregano rhizosphere, identified, and functionally characterized. All the isolates exhibited multiple PGP traits such as IAA production, phosphate solubilization, and stress tolerance. Among them, Streptomyces sp. B18, emerging as the most promising, was used in oregano seed germination tests. These results provide evidence that S. violaceoruber and K. rhizophila enhance oregano and tomato growth and also modulate their metabolome. Furthermore, oregano hydrolates obtained from plants inoculated with the actinobacterial consortium and from uninoculated plants showed different effects on global DNA methylation in undifferentiated Caco-2 cells. In particular, hydrolates derived from inoculated plants induced marked hypomethylation, a phenomenon that could promote an overall genomic instability. These promising results underline the possibility of considering consortium-hydrolates as potent chemotherapeutic agents, capable of stimulating non-apoptotic cell death. Hence, the two actinomycetota represent promising strains for improving crop performance and, potentially, for the targeted modulation of secondary metabolite production in Mediterranean plants. Thus, through the integration of microbial, plant, and environmental health, we aim to develop innovative solutions aligned with the ‘One Health’ mission.