Taxonomy-guided selection of Paraburkholderia busanensis sp. nov.: a versatile biocontrol agent with mycophagy against Colletotrichum scovillei causing pepper anthracnose.

Abstract

This study introduces a novel approach based on the taxonomy-guided selection of bacterial biocontrol agents from a known beneficial taxonomic group. Following 16S rRNA screening, we focused on the genus Paraburkholderia, which harbors strains with large genomes and versatile benefits to plants. A strain designated P39 was selected, identified, and characterized for its biocontrol activity against Colletotrichum scovillei. Strain P39 exhibited antagonism against C. scovillei by producing compounds, including volatiles, with antifungal activity, both in vitro and on pepper fruits. Genomic, physiological, and biochemical analyses revealed that the selected strain represents a novel species, named Paraburkholderia busanensis. Genomic analyses provided insights into the fitness and biocontrol activities of the selected strains. Moreover, P39 displays mycophagy, consuming fungal mycelia and transforming them into bacterial biomass, particularly in nutrient-poor media supplemented with fungal mycelia. The genome harbored chitin and N-acetylglucosamine utilization genes, suggesting a proposed pathway for the utilization of fungal cells as a nutrient source. Microscopic observations further supported the ability of this strain to rupture and damage fungal hyphae, depriving them of their cellular constituents. This study successfully demonstrated the implementation of a taxonomy-guided approach for the selection of bacterial strains for biocontrol. These findings contribute to our understanding of biocontrol strategies, bacteria-fungi interactions, and the identification of Paraburkholderia busanensis sp. nov. as a potential candidate for the biocontrol of pepper anthracnose. Additionally, this strain serves as a valuable resource for antifungal compounds and volatiles, and for the study of bacteria-fungal interactions and mycophagy. IMPORTANCE Traditional control methods for postharvest diseases rely on fungicides, which cause human health and environmental concerns. This study introduces a taxonomy-guided strategy for selecting biocontrol agents. By focusing on Paraburkholderia group, which harbors diverse plant-beneficial strains, the inadvertent selection of harmful strains was circumvented, thereby obviating the need for laborious in vitro screening assays. A highly promising candidate, strain P39, has been identified, exhibiting remarkable biocontrol activity against Colletotrichum scovillei. Through comprehensive genomic, physiological, and biochemical analyses, P39 was characterized as a novel species within the Paraburkholderia genus and designated Paraburkholderia busanensis. Moreover, these findings deepen our understanding of bacterial-fungal interactions, as they elucidate a potential pathway for the utilization of fungal chitin, thereby enhancing our understanding of bacterial mycophagy. P. busanensis is a promising source of antifungal volatiles and putative novel secondary metabolites.