Soil microbiome bacteria protect plants against filamentous fungal infections via intercellular contacts

L Long Lin D Danyu Shen (Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University) X Xiaolong Shao (Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University) Y Yicheng Yang (Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University) L Li Li C Caihong Zhong (Engineering Laboratory for Kiwifruit Industrial Technology, Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences) J Jiandong Jiang (Department of Microbiology, Key Lab of Microbiology for Agricultural Environment, College of Life Sciences, Nanjing Agricultural University) M Mengcen Wang (State Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University) G Guoliang Qian (Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University)

Abstract

Bacterial–fungal interaction (BFI) has significant implications for the health of host plants. While the diffusible antibiotic metabolite-mediated competition in BFI has been extensively characterized, the impact of intercellular contact remains largely elusive. Here, we demonstrate that the intercellular contact is a prevalent mode of interaction between beneficial soil bacteria and pathogenic filamentous fungi. By generating antibiotics-deficient mutants in two common soil bacteria, Lysobacter enzymogenes and Pseudomonas fluorescens , we show that antibiotics-independent BFI effectively inhibits pathogenic fungi. Furthermore, transcriptional and genetic evidence revealed that this antibiotics-independent BFI relies on intercellular contact mediated by the type VI secretion system (T6SS), which may facilitate the translocation of bacterial toxic effectors into fungal cells. Finally, by using a “conidia enrichment” platform, we found that T6SS-mediated fungal inhibition resulting from intercellular contact naturally occurs within the soil microbiome, particularly represented by Pseudomonas fulva . Overall, these results demonstrate that bacteria from the soil microbiome can protect host plants from fungal infection through antibiotics-independent intercellular contacts, thus revealing a naturally occurring and ecologically important mode of BFI in agricultural contexts.

Article Details

Volume / Issue Vol. 122, Issue 3
Published January 21, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (9)

L

Long Lin

D

Danyu Shen

Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University

X

Xiaolong Shao

Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University

Y

Yicheng Yang

Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University

L

Li Li

C

Caihong Zhong

Engineering Laboratory for Kiwifruit Industrial Technology, Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, Chinese Academy of Sciences

J

Jiandong Jiang

Department of Microbiology, Key Lab of Microbiology for Agricultural Environment, College of Life Sciences, Nanjing Agricultural University

M

Mengcen Wang

State Key Laboratory of Rice Biology and Breeding, Ministry of Agricultural and Rural Affairs Laboratory of Molecular Biology of Crop Pathogens and Insects, Zhejiang University

G

Guoliang Qian

Department of Plant Pathology, Key Laboratory of Plant Immunity, Key Laboratory of Integrated Management of Crop Diseases and Pests, College of Plant Protection, Nanjing Agricultural University