Abstract
The soil bacterium Bacillus thuringiensis is a pathogen of insects and nematodes and is very closely related to, if not the same species as, Bacillus cereus and Bacillus anthracis. The defining characteristic of B. thuringiensis that sets it apart from B. cereus and B. anthracis is the production of crystal (Cry) proteins, which are pore-forming toxins or pore-forming proteins (PFPs). Although it is known that PFPs are important virulence factors since their elimination results in reduced virulence of many pathogenic bacteria, the functions by which PFPs promote virulence are incompletely understood. Here we study the effect of Cry proteins in B. thuringiensis pathogenesis of the nematode Caenorhabditis elegans. We find that whereas B. thuringiensis on its own is not able to infect C. elegans, the addition of the PFP Cry protein, Cry5B, results in a robust lethal infection that consumes the nematode host in 1–2 days, leading to a “Bob” or bag-of-bacteria phenotype. Unlike other infections of C. elegans characterized to date, the infection by B. thuringiensis shows dose-dependency based on bacterial inoculum size and based on PFP concentration. Although the infection process takes 1–2 days, the PFP-instigated infection process is irreversibly established within 15 minutes of initial exposure. Remarkably, treatment of C. elegans with Cry5B PFP is able to instigate many other Bacillus species, including B. anthracis and even “non-pathogenic” Bacillus subtilis, to become lethal and infectious agents to C. elegans. Co-culturing of Cry5B-expressing B. thuringiensis with B. anthracis can result in lethal infection of C. elegans by B. anthracis. Our data demonstrate that one potential property of PFPs is to sensitize the host to bacterial infection and further that C. elegans and probably other roundworms can be common hosts for B. cereus-group bacteria, findings with important ecological and research implications.
Highlights
The Bacillus cereus group of bacteria comprises six species, including three highly related species, B. cereus sensu stricto, B. anthracis and B. thuringiensis, which are sometimes considered a single species [1,2,3]
In our numerous studies of nematicidal Cry proteins in the absence of B. thuringiensis but in the presence of its standard laboratory food source, Escherichia coli, we have found that Cry proteins produce a dose-dependent mortality in nematodes but do not promote an E. coli infection
We investigated what would happen if we fed C. elegans Cry5B, a Cry protein that forms pores in membranes [13], in the presence of B. thuringiensis
Summary
The Bacillus cereus group of bacteria comprises six species, including three highly related species, B. cereus sensu stricto, B. anthracis and B. thuringiensis, which are sometimes considered a single species [1,2,3] Closely related, these bacteria are associated with very different diseases. B. anthracis is the causative agent of anthrax [4], B. cereus can cause food poisoning and various opportunistic and nosocomial infections [5], and B. thuringiensis is an invertebrate-specific pathogen [6] The relationship between these three closely related species of Bacillus in the wild, e.g. how they replicate in the soil environment and what environmental niches they occupy relative to one another, has been the subject of much speculation [7,8]. Purified Cry proteins alone, even in the absence of B. thuringiensis, produce dose-dependent lethality in invertebrates, and as such can be expressed in transgenic crops to control insect pests
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