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

Author:

Lin Long1,Shen Danyu1ORCID,Shao Xiaolong1,Yang Yicheng1,Li Li2ORCID,Zhong Caihong2,Jiang Jiandong3,Wang Mengcen45,Qian Guoliang1ORCID

Affiliation:

1. 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

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

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

4. 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

5. Department of Plant Protection, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Pesticide and Environmental Toxicology, College of Agriculture and Biotechnology, Zhejiang 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.

Publisher

Proceedings of the National Academy of Sciences

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