Transcriptional changes when Myxococcus xanthus preys on Escherichia coli suggest myxobacterial predators are constitutively toxic but regulate their feeding.

Paul G Livingstone,David E Whitworth,Andrew D Millard,Martin T Swain

doi:10.1099/mgen.0.000152

Abstract

Predation is a fundamental ecological process, but within most microbial ecosystems the molecular mechanisms of predation remain poorly understood. We investigated transcriptome changes associated with the predation of Escherichia coli by the myxobacterium Myxococcus xanthus using mRNA sequencing. Exposure to pre-killed prey significantly altered expression of 1319 predator genes. However, the transcriptional response to living prey was minimal, with only 12 genes being significantly up-regulated. The genes most induced by prey presence (kdpA and kdpB, members of the kdp regulon) were confirmed by reverse transcriptase quantitative PCR to be regulated by osmotic shock in M. xanthus, suggesting indirect sensing of prey. However, the prey showed extensive transcriptome changes when co-cultured with predator, with 40 % of its genes (1534) showing significant changes in expression. Bacteriolytic M. xanthus culture supernatant and secreted outer membrane vesicles (OMVs) also induced changes in expression of large numbers of prey genes (598 and 461, respectively). Five metabolic pathways were significantly enriched in prey genes up-regulated on exposure to OMVs, supernatant and/or predatory cells, including those for ribosome and lipopolysaccharide production, suggesting that the prey cell wall and protein production are primary targets of the predator’s attack. Our data suggest a model of the myxobacterial predatome (genes and proteins associated with predation) in which the predator constitutively produces secretions which disable its prey whilst simultaneously generating a signal that prey is present. That signal then triggers a regulated feeding response in the predator.

Highlights

Across the natural world, predation is a virtually ubiquitous ecological phenomenon which drives the evolution of predator and prey organisms
We investigated transcriptome changes associated with the predation of Escherichia coli by the ‘wolf-pack’ myxobacterial predator Myxococcus xanthus using mRNA sequencing
Reads were mapped to the genomes of M. xanthus and E. coli and an FPKM value was assigned to each gene reflecting its relative expression level

Summary

Introduction

Predation is a virtually ubiquitous ecological phenomenon which drives the evolution of predator and prey organisms. The soil-dwelling myxobacteria are a well-described order of predatory bacteria, which feed co-operatively on a broad range of prey organisms [3,4,5]. Myxobacterial molecular genetics has been studied for several decades, knowledge of the mechanisms involved in their predatory activity remains sparse [6]. Numerous studies have shown that myxobacteria exhibit predatory activity against a broad range of prey, including Gram-negative bacteria, Gram-positive bacteria and fungi [4, 5, 7, 8]. The broad prey range of myxobacteria is believed to be a consequence of their mode of predation, described as ‘wolf-pack’ predation [8, 10].

Methods

Results

Conclusion