An intrinsic mechanism for coordinated production of the contact-dependent and contact-independent weapon systems in a soil bacterium.

Mingming Yang,Xi Shen,Guoliang Qian,Danyu Shen,Nianda Yang,Shan-Ho Chou,Shuangshuang Ren,Bingxin Wang,Sen Han,Erh-Min Lai

doi:10.1371/journal.ppat.1008967

Abstract

Soil bacteria possess multiple weapons to fend off microbial competitors. Currently, we poorly understand the factors guiding bacterial decisions about weapon systems deployment. In this study, we investigated how such decisions are made by the soil bacterium Lysobacter enzymogenes, used in antifungal plant protection. We found that weapons production is guided by environmental cues. In rich media, which likely mimic environments crowded with other microbes, L. enzymogenes produces a contact-dependent weapon, type six secretion system (T6SS). In nutrient-poor media, likely dominated by filamentous oomycetes and fungi, L. enzymogenes synthesizes and secretes a heat-stable antifungal factor (HSAF), a contact-independent weapon. Surprisingly, the T6SS inner tube protein Hcp is accumulated intracellularly even in nutrient-poor media, when the T6SS is not assembled. We found that Hcp interacts with the transcription factor Clp required for activating HSAF biosynthesis operon expression. Hcp protects Clp from binding to c-di-GMP, an intracellular second messenger inhibiting DNA binding. The increased concentration of c-di-GMP-free Clp thus leads to higher gene expression and HSAF production. Therefore, when the contact-dependent weapon, T6SS, is not in use, accumulation of one of its structural components, Hcp, serves as a signal to enhance production of the contact-independent weapon, HSAF. The uncovered environment-dependent and auto-regulatory mechanisms shed light on the processes governing deployment of various weapon systems in environmental bacteria.

Highlights

Soil bacteria are surrounded by diverse competitors that include other bacteria, fungi, oomycetes and protists [1, 2]
We found that Hcp interacts with the transcription factor Clp required for activating heat-stable antifungal factor (HSAF) biosynthesis operon expression
We found that T6SS and HSAF are produced under different nutrient conditions, where the density and type of microbial competitors of L. enzymogenes likely differ

Summary

Introduction

Soil bacteria are surrounded by diverse competitors that include other bacteria, fungi, oomycetes and protists [1, 2]. To fend off these competitors, bacteria deploy various toxins, which are either secreted into the surrounding medium (contact-independent weapons) or injected directly into the competitor cell (contact-dependent weapons). T6SS is commonly used by the proteobacteria for contact-induced killing. Upon cell-cell contact, an engaged T6SS injects a toxin-loaded shell, known as inner tube, into the target cell by piercing though its cell wall and membranes [4, 5]. T6SS toxins possess diverse killing modalities that are effective primarily against bacteria [6,7,8]. Serratia marcescens, delivers antifungal effectors against Saccharomyces cerevisiae and pathogenic Candida albicans [9, 10]

Methods

Results

Discussion

Conclusion