Widely targeted metabolomic, transcriptomic, and metagenomic profiling reveal microbe–plant–metabolic reprogramming patterns mediated by Streptomyces pactum Act12 enhance the fruit quality of Capsicum annuum L.

[Display omitted] • Soil application of Streptomyces pactum enhances pepper fruit quality in the field. • Metabolic reprogramming is deciphered via transcriptomic and metabolomic analyses. • Fruit metabolic reprogramming is coupled with rhizosphere microbiota reshaping. • Microbe-mediated fruit quality enhancement is clarified from an ecological perspective. Plant growth-promoting rhizobacteria, such as Streptomyces pactum Act12, promote crop growth and stress resistance, but their contribution to fruit quality is still poorly understood. Herein we conducted a field experiment to ascertain the effects of S. pactum Act12-mediated metabolic reprogramming and underlying mechanisms in pepper (Capsicum annuum L.) fruit based on widely targeted metabolomic and transcriptomic profiling. We additionally performed metagenomic analysis to elucidate the potential relationship between S. pactum Act12-mediated reshaping of rhizosphere microbial communities and pepper fruit quality. Soil inoculation with S. pactum Act12 considerably increased the accumulation of capsaicinoids, carbohydrates, organic acids, flavonoids, anthraquinones, unsaturated fatty acids, vitamins, and phenolic acids in pepper fruit samples. Consequently, fruit flavor, taste, and color were modified, accompanied by elevated contents of nutrients and bioactive compounds. Increased microbial diversity and recruitment of potentially beneficial taxa were observed in inoculated soil samples, with crosstalk between microbial gene functions and pepper fruit metabolism. The reformed structure and function of rhizosphere microbial communities were closely associated with pepper fruit quality. Our findings indicate that S. pactum Act12-mediated interactions between rhizosphere microbial communities and pepper plants are responsible for intricate fruit metabolic reprogramming patterns, which enhance not only overall fruit quality but also consumer acceptability. [ABSTRACT FROM AUTHOR]