Soil microorganisms can mediate the occurrence of plant diseases. Potato common scab (CS) is a refractory disease caused by pathogenic Streptomyces that occurs worldwide, but little is known about the interactions between CS and the soil microbiome. In this study, four soil-root system compartments (geocaulosphere soil (GS), rhizosphere soil (RS), root-zone soil (ZS), and furrow soil (FS)) were analyzed for potato plants with naturally high (H) and low (L) scab severity levels. We aimed to determine the composition and putative function of the soil microbiome associated with potato CS. The copy numbers of the scab phytotoxin biosynthetic gene txtAB and the bacterial 16S rRNA gene as well as the diversity and composition of each of the four soil-root system compartments were examined; GS was the only compartment that exhibited significant differences between the H and L groups. Compared to the H group, the L group exhibited a lower txtAB gene copy number, lower bacterial 16S copy number, higher diversity, higher co-occurrence network complexity, and higher community function similarity within the GS microbiome. The community composition and function of the GS samples were further revealed by shotgun metagenomic sequencing. Variovorax, Stenotrophomonas, and Agrobacterium were the most abundant genera that were significantly and positively correlated with the scab severity level, estimated absolute abundance (EAA) of pathogenic Streptomyces, and txtAB gene copy number. In contrast, Geobacillus, Curtobacterium, and unclassified Geodermatophilaceae were significantly negatively correlated with these three parameters. Compared to the function profiles in the L group, several genes involved in “ABC transporters,” the “bacterial secretion system,” “quorum sensing (QS),” “nitrogen metabolism,” and some metabolism by cytochrome P450 were enriched in the H group. In contrast, some antibiotic biosynthesis pathways were enriched in the L group. Based on the differences in community composition and function, a simple model was proposed to explain the putative relationships between the soil microbiome and CS occurrence. The GS microbiome was closely associated with CS severity in the soil-root system, and the occurrence of CS was accompanied by changes in community composition and function. The differential functions provide new clues to elucidate the mechanism underlying the interaction between CS occurrence and the soil microbiome, and varying community compositions provide novel insights into CS occurrence.

This study demonstrates that halophyte root-associated microorganisms can promote crop tolerance to salt stress and clarify the mechanism by which the strains work in rhizosphere soil. The links among salt-tolerant microorganisms, soil, and plants established in this study can inform strategies for improving crop cultivation in salinized lands.