Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots

TY - JOUR

T1 - Fusarium oxysporum Disrupts Microbiome-Metabolome Networks in Arabidopsis thaliana Roots

AU - Kudjordjie, Enoch Narh

AU - Hooshmand, Kourosh

AU - Sapkota, Rumakanta

AU - Darbani, Behrooz

AU - Fomsgaard, Inge S.

AU - Nicolaisen, Mogens

PY - 2022/8

Y1 - 2022/8

N2 - While the plant host metabolome drives distinct enrichment of detrimental and beneficial members of the microbiome, the mechanistic interomics relationships remain poorly understood. Here, we studied microbiome and metabolome profiles of two Arabidopsis thaliana accessions after Fusarium oxysporum f.sp. mathioli (FOM) inoculation, Landsberg erecta (Ler-0) being susceptible and Col-0 being resistant against FOM. By using bacterial and fungal amplicon sequencing and targeted metabolite analysis, we observed highly dynamic microbiome and metabolome profiles across FOM host progression, while being markedly different between FOM-inoculated and noninoculated Col-0 and Ler-0. Co-occurrence network analysis revealed more robust microbial networks in the resistant Col-0 compared to Ler-0 during FOM infection. Correlation analysis revealed distinct metabolite-OTU correlations in Ler-0 compared with Col-0 which could possibly be explained by missense variants of the Rfo3 and Rlp2 genes in Ler-0. Remarkably, we observed positive correlations in Ler-0 between most of the analyzed metabolites and the bacterial phyla Proteobacteria, Bacteroidetes, Planctomycetes, Acidobacteria, and Verrucomicrobia, and negative correlations with Actinobacteria, Firmicutes, and Chloroflexi. The glucosinolates 4-methyoxyglucobrassicin, glucoerucin and indole-3 carbinol, but also phenolic compounds were strongly correlating with the relative abundances of indicator and hub OTUs and thus could be active in structuring the A. thaliana root-associated microbiome. Our results highlight interactive effects of host plant defense and root-associated microbiota on Fusarium infection and progression. Our findings provide significant insights into plant interomic dynamics during pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control.

AB - While the plant host metabolome drives distinct enrichment of detrimental and beneficial members of the microbiome, the mechanistic interomics relationships remain poorly understood. Here, we studied microbiome and metabolome profiles of two Arabidopsis thaliana accessions after Fusarium oxysporum f.sp. mathioli (FOM) inoculation, Landsberg erecta (Ler-0) being susceptible and Col-0 being resistant against FOM. By using bacterial and fungal amplicon sequencing and targeted metabolite analysis, we observed highly dynamic microbiome and metabolome profiles across FOM host progression, while being markedly different between FOM-inoculated and noninoculated Col-0 and Ler-0. Co-occurrence network analysis revealed more robust microbial networks in the resistant Col-0 compared to Ler-0 during FOM infection. Correlation analysis revealed distinct metabolite-OTU correlations in Ler-0 compared with Col-0 which could possibly be explained by missense variants of the Rfo3 and Rlp2 genes in Ler-0. Remarkably, we observed positive correlations in Ler-0 between most of the analyzed metabolites and the bacterial phyla Proteobacteria, Bacteroidetes, Planctomycetes, Acidobacteria, and Verrucomicrobia, and negative correlations with Actinobacteria, Firmicutes, and Chloroflexi. The glucosinolates 4-methyoxyglucobrassicin, glucoerucin and indole-3 carbinol, but also phenolic compounds were strongly correlating with the relative abundances of indicator and hub OTUs and thus could be active in structuring the A. thaliana root-associated microbiome. Our results highlight interactive effects of host plant defense and root-associated microbiota on Fusarium infection and progression. Our findings provide significant insights into plant interomic dynamics during pathogen invasion and could possibly facilitate future exploitation of microbiomes for plant disease control.

KW - plant pathogen

KW - root microbiome

KW - glucosinolates

KW - phenylpropanoids

KW - phytohormones

KW - microbial co-occurrence networks

KW - plant resistance

KW - DEGRADATION-PRODUCTS

KW - DISEASE-RESISTANCE

KW - BACTERIAL

KW - DIVERSITY

KW - RHIZOSPHERE

KW - REVEALS

KW - ACID

KW - GROWTH

KW - STREPTOMYCES

KW - STABILITY

KW - Plant Diseases/microbiology

KW - Arabidopsis/genetics

KW - Metabolome

KW - Fusarium/genetics

KW - Microbiota

KW - Bacteria

U2 - 10.1128/spectrum.01226-22

DO - 10.1128/spectrum.01226-22

M3 - Journal article

C2 - 35766498

SN - 2165-0497

VL - 10

JO - Microbiology Spectrum

JF - Microbiology Spectrum

IS - 4

M1 - e01226-22

ER -