Soil Microbiome Mechanisms For Potato Common Scab Development

The healthy and sustainable development of the potato industry is not only important for food security in China,but also for the successful implementation of the rural revitalisation strategy.Potato common scab(PCS),caused by the pathogenic Streptomyces spp.,is one of the most important soil-borne diseases threatening the potato industry.The pathogens are both seed-and soil-borne and are extremely difficult to control.Some pathogens can also infect rhizomatous plants such as radish,carrot,sugar beet and sweet potato.Soil-borne plant diseases are closely influenced by the soil microbiome,and the microbiome is considered to be the key to the next green revolution.Regulation of soil microbial communities has been reported to control PCS development.However,the mechanism of the soil microbiome on the development of PCS is still largely unclear.Two field experiments were conducted in this study,the first in a continuous cropping potato field in Jiaozhou,Shandong Province,and the second in four continuous cropping potato fields with significantly different soil conditions in Jiaozhou and Tengzhou,Shandong Province.Soil samples were collected at different PCS severity levels(H:high PCS severity;L:low PCS severity)and the relationship between the soil microbiome and the PCS severity was systematically investigated using cultivation-independent microbiome methods,and the effect of specific microbial taxa on the PCS pathogen was verified in combination with cultivation-dependent methods.The main findings were as follows.(1)The bacterial community characteristics of geocaulosphere soil differ significantly between H and L.For the first field experiment,the bacterial communities of potato geocaulosphere soil(GS;soil within 2 mm of the tuber surface),rhizosphere soil(RS;soil within 2 mm of the root surface),root-zone soil(ZS;soil at a depth of 5-15 cm in the plant growth zone)and furrow soil(FS;soil at a depth of 5-15 cm in the furrow next to the plant)were compared with different PCS severity.The results showed significant differences in the abundance of pathogenic Streptomyces,txt AB copy numbers(characterising absolute pathogen abundance),bacterial 16S r RNA gene copy numbers(characterising absolute bacterial abundance),bacterial?-diversity indices(OTU numbers,Chao1 and Shannon)and community compositions in GS,while no significant differences were found in the other three types of soil samples.Compared to GSH,GSL had lower toxin synthesis gene txt AB copy number,lower bacterial 16S r RNA gene copy number,higher bacterial?-diversity indices,more complex bacterial co-occurrence networks and higher microbial functional similarity.(2)Specific microbial community members and functions in GS are associated with PCS severity.A further analysis of the GS microbial community was carried out using shotgun metagenomic sequencing.Correlation analysis showed that the absolute abundance of four genera,Stenotrophomonas,Agrobacterium,Sphingobium and Streptomyces,were highly correlated with PCS severity,pathogen abundance and txt AB gene copy number(Spearman,?>0.8,P<0.05),whereas the absolute abundance of three genera,Geobacillus,Curtobacterium and unclassified Geodermatophilaceae,were significantly negatively correlated with all three PCS parameter(Spearman,?<-0.6,P<0.05).KEGG functional enrichment analysis showed that the pathways enriched in GSH were mainly“nitrogen metabolism”,“drug metabolism-cytochrome P450”,“metabolism of xenobiotics by cytochrome P450”,“steroid biosynthesis”,“ABC transporters”and“bacterial secretion system”.In contrast,the pathways enriched in GSL were mainly“carbohydrate metabolism”,“energy metabolism”and some sugar and antibiotic biosynthetic pathways such as acarbose,streptomycin,validamycin,neomycin,kanamycin and gentamicin.(3)The relationship between GS bacterial communities and PCS severity levels exhibits a generalised pattern across differing soil conditions.PCo A and ADONIS analyses showed that the physicochemical properties,bacterial communities,microeukaryotic communities and archaeal communities of the bulk soil(BS;soil at 5-15 cm depth in the plant growth zone)of the second field experiment differed significantly among fields.The different physicochemical properties and microbial communities of BS significantly affected the GS bacterial communities(R~2=0.25,P=0.001),microeukaryotic communities(R~2=0.27,P=0.001)and archaeal communities(R~2=0.62,P=0.001).But the GS bacterial communities still responded to PCS severity under the different soil conditions(R~2=0.20,P=0.001).In contrast to the bacterial community,the microeukaryotic(R~2=0.08,P=0.002)and archaeal communities(R~2=0.04,P=0.087)showed little difference between H and L.The random-forest model showed that even under different soil conditions,the GS bacterial communities remained an accurate(100%)predictor of PCS severity.(4)Soil bacterial communities demonstrate the highest explanatory power for PCS severity.Correlation and VPA analyses together showed that the GS bacterial communities explained the highest variation of PCS severity(68.8%),followed by pathogen abundance(56.3%),both of which were much higher than microeukaryotic communities(19.1%)and archaeal communities(12.2%).The mediating effects analysis of structural equation modelling showed that both direct(pathogen abundance-PCS severity)and indirect(pathogen abundance-bacterial communities-PCS severity)effects of pathogen abundance on PCS severity were significant,with the indirect effect(0.42)being stronger than the direct effect(0.32).The BS bacterial communities(45.5%)and physicochemical properties(42.3%)showed high explanatory power for the GS bacterial communities,however,the BS pathogen abundance had almost zero explanatory power for the GS microbial communities,pathogen abundance and PCS severity.(5)When PCS occurs,GS accumulates specific beneficial microorganisms that inhibit the growth and virulence effects of the pathogen.Correlation analysis showed that a certain number of OTUs were significantly associated with pathogen OTUs in each field(P<0.05),with JD,JF,TX and TZ having 56,160,83 and 238,respectively.Further statistical analysis revealed that 34 genera,in three or more fields,consistently contained OTUs that were significantly correlated with pathogen OTUs.Twelve of these genera were isolated from the potato epidermis and its surface soil in culture experiment.Antagonism experiment and radish seedling growth experiment showed that a high proportion(20/60)of strains,mainly belonging to Chryseobacterium,Stenotrophomonas,Sphingobacterium,Sphingobium and Bacillus,were able to significantly inhibit the growth of the pathogen and alleviate the inhibitory effect of the pathogen on radish seedling growth.This study clarifies the relationship between the soil microbiome and the PCS severity;reveals that PCS severity is accompanied by changes in GS microbial community compositions and functions;highlights that bacterial community composition explains PCS severity better than pathogen abundance;and demonstrates that specific pathogen-suppressive microorganisms are significantly enriched in GS following the PCS occurs.The study provides a preliminary analysis of the soil microbiome mechanisms underlying the development of PCS.