Ecological consequences of ingestion of Bacillus cereus on Bacillus thuringiensis infections and on the gut flora of a lepidopteran host

Raymond, Ben; Lijek, Rebeccah S.; Griffiths, Robert I.; Bonsall, Michael B.

doi:10.1016/j.jip.2008.04.007

Cited by 32 publications

(30 citation statements)

References 53 publications

(60 reference statements)

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“…As previously suggested (28), it is probable that the array of antibiotics (24), bacteriocins (4), and quorum quenchers (23) produced by B. thuringiensis may confer a competitive advantage over gut microbes that coinvade the hemocoel and compete for the consumption of the host cadaver. Facultatively pathogenic gut bacteria may synergize Cry protein toxicity or the toxicity of B. thuringiensis strains which are attenuated versus a particular species of insect.…”

Section: Discussionmentioning

confidence: 92%

Gut Bacteria Are Not Required for the Insecticidal Activity of Bacillus thuringiensis toward the Tobacco Hornworm, Manduca sexta

Johnston

Crickmore

2009

Appl Environ Microbiol

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It was recently proposed that gut bacteria are required for the insecticidal activity of the Bacillus thuringiensis-based insecticide, DiPel, toward the lepidopterans Manduca sexta, Pieris rapae, Vanessa cardui, and Lymantria dispar. Using a similar methodology, it was found that gut bacteria were not required for the toxicity of DiPel or Cry1Ac or for the synergism of an otherwise sublethal concentration of Cry1Ac toward M. sexta. The toxicities of DiPel and of B. thuringiensis HD73 Cry ؊ spore/Cry1Ac synergism were attenuated by continuously exposing larvae to antibiotics before bioassays. Attenuation could be eliminated by exposing larvae to antibiotics only during the first instar without altering larval sterility. Prior antibiotic exposure did not attenuate Cry1Ac toxicity. The presence of enterococci in larval guts slowed mortality resulting from DiPel exposure and halved Cry1Ac toxicity but had little effect on B. thuringiensis HD73 Cry ؊ spore/Cry1Ac synergism. B. thuringiensis Cry ؊ cells killed larvae after intrahemocoelic inoculation of M. sexta, Galleria mellonella, and Spodoptera litura and grew rapidly in plasma from M. sexta, S. litura, and Tenebrio molitor. These findings suggest that gut bacteria are not required for B. thuringiensis insecticidal activity toward M. sexta but that B. thuringiensis lethality is reduced in larvae that are continuously exposed to antibiotics before bioassay.Bacillus thuringiensis has long been regarded as a bona fide entomopathogen that can produce an array of virulence factors including insecticidal parasporal crystal (Cry) toxins, vegetative insecticidal proteins, phospholipases, immune inhibitors, and antibiotics (31). B. thuringiensis establishes lethal infections in many insect species after intrahemocoelic inoculation (9,10,14,26,31), and the insecticidal activity of Cry toxins, which lyse the intestinal epithelium, can be synergized by the presence of viable B. thuringiensis spores (31). In each instance, synergism has been attributed to hemocoelic infection by B. thuringiensis.A novel hypothesis (6, 7) proposed that B. thuringiensis is incapable of killing Lymantria dispar, Manduca sexta, Pieris rapae, or Vanessa cardui in the absence of gut bacteria. Prior exposure of L. dispar larvae to a combination of four antibiotics severely reduced the subsequent toxicity of the B. thuringiensis-based (spores and Cry toxins) bioinsecticide, DiPel (Valent BioSciences) (6). Both larval susceptibility to B. thuringiensis and the number of culturable gut bacteria were found to be negatively correlated with the concentration of antibiotics to which larvae were previously exposed. Furthermore, a total reduction in larval susceptibility was coincident with the elimination of any detectable gut bacteria. Experimental reinfection with Enterobacter sp. strain NAB3, found in the guts of some populations of L. dispar larvae, was found to rescue the toxicity of B. thuringiensis, whereas reinfection with Enterococcus casseliflavus and Staphylococcus xylosus did not. It was also sho...

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Section: Discussionmentioning

confidence: 92%

Gut Bacteria Are Not Required for the Insecticidal Activity of Bacillus thuringiensis toward the Tobacco Hornworm, Manduca sexta

Johnston

Crickmore

2009

Appl Environ Microbiol

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“…In chickens, infection of Campylobacter jejuni resulted in the loss of specific bacterial lineages and more similar bacterial communities among infected chickens relative to control chickens (Johansen et al, 2006). Similar effects have also been seen in other insects; for example, infection of antibiotic-secreting bacteria from the Bacillus cereus group reduced the diversity of gut flora in moth larvae (Raymond et al, 2008).…”

mentioning

confidence: 61%

Yersinia pestis infection and laboratory conditions alter flea-associated bacterial communities

et al. 2012

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We collected Oropsylla montana from rock squirrels, Spermophilus varigatus, and infected a subset of collected fleas with Yersinia pestis, the etiological agent of plague. We used bar-tagged DNA pyrosequencing to characterize bacterial communities of wild, uninfected controls and infected fleas. Bacterial communities within Y. pestis-infected fleas were substantially more similar to one another than communities within wild or control fleas, suggesting that infection alters the bacterial community in a directed manner such that specific bacterial lineages are severely reduced in abundance or entirely eliminated from the community. Laboratory conditions also significantly altered flea-associated bacterial communities relative to wild communities, but much less so than Y. pestis infection. The abundance of Firmicutes decreased considerably in infected fleas, and Bacteroidetes were almost completely eliminated from both the control and infected fleas. Bartonella and Wolbachia were unaffected or responded positively to Y. pestis infection.

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“…In earthworms, germination seems to be restricted to the gut and sporulation may occur after defecation (Hendriksen & Hansen, 2002;Swiecicka, 2008). Multiplication and sporulation seem to be also associated with death of their hosting animal, which may have been caused by the bacterium itself (B. thuringiensis for insects, B. anthracis in mammals), or in the case of B. cereus sensu stricto during co-infection of insects with B. thuringiensis (Raymond, Lijek, Griffiths, & Bonsall, 2008). Consequently this suggests that climate change may influence the viability of B. cereus in two aspects.…”

Section: Environment Of Sporulation and Spore Propertiesmentioning

confidence: 99%

Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment

Carlin

Brillard

Broussolle

et al. 2010

Food Research International

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Ecological consequences of ingestion of Bacillus cereus on Bacillus thuringiensis infections and on the gut flora of a lepidopteran host

Cited by 32 publications

References 53 publications

Gut Bacteria Are Not Required for the Insecticidal Activity of Bacillus thuringiensis toward the Tobacco Hornworm, Manduca sexta

Gut Bacteria Are Not Required for the Insecticidal Activity of Bacillus thuringiensis toward the Tobacco Hornworm, Manduca sexta

Yersinia pestis infection and laboratory conditions alter flea-associated bacterial communities

Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment

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