Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response
ABSTRACT Competitive interactions between bacteria reveal physiological adaptations that benefit fitness. Bacillus subtilis is a Gram-positive species with several adaptive mechanisms for competition and environmental stress. Biofilm formation, sporulation, and motility are the outcomes of widesprea...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-02-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00586-17 |
| _version_ | 1828953638954860544 |
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| author | Yongjin Liu Steven Kyle Paul D. Straight |
| author_facet | Yongjin Liu Steven Kyle Paul D. Straight |
| author_sort | Yongjin Liu |
| collection | DOAJ |
| description | ABSTRACT Competitive interactions between bacteria reveal physiological adaptations that benefit fitness. Bacillus subtilis is a Gram-positive species with several adaptive mechanisms for competition and environmental stress. Biofilm formation, sporulation, and motility are the outcomes of widespread changes in a population of B. subtilis. These changes emerge from complex, regulated pathways for adapting to external stresses, including competition from other species. To identify competition-specific functions, we cultured B. subtilis with multiple species of Streptomyces and observed altered patterns of growth for each organism. In particular, when plated on agar medium near Streptomyces venezuelae, B. subtilis initiates a robust and reproducible mobile response. To investigate the mechanistic basis for the interaction, we determined the type of motility used by B. subtilis and isolated inducing metabolites produced by S. venezuelae. Bacillus subtilis has three defined forms of motility: swimming, swarming, and sliding. Streptomyces venezuelae induced sliding motility specifically in our experiments. The inducing agents produced by S. venezuelae were identified as chloramphenicol and a brominated derivative at subinhibitory concentrations. Upon further characterization of the mobile response, our results demonstrated that subinhibitory concentrations of chloramphenicol, erythromycin, tetracycline, and spectinomycin all activate a sliding motility response by B. subtilis. Our data are consistent with sliding motility initiating under conditions of protein translation stress. This report underscores the importance of hormesis as an early warning system for potential bacterial competitors and antibiotic exposure. IMPORTANCE Antibiotic resistance is a major challenge for the effective treatment of infectious diseases. Identifying adaptive mechanisms that bacteria use to survive low levels of antibiotic stress is important for understanding pathways to antibiotic resistance. Furthermore, little is known about the effects of individual bacterial interactions on multispecies communities. This work demonstrates that subinhibitory amounts of some antibiotics produced by streptomycetes induce active motility in B. subtilis, which may alter species interaction dynamics among species-diverse bacterial communities in natural environments. The use of antibiotics at subinhibitory concentrations results in many changes in bacteria, including changes in biofilm formation, small-colony variants, formation of persisters, and motility. Identifying the mechanistic bases of these adaptations is crucial for understanding how bacterial communities are impacted by antibiotics. |
| first_indexed | 2024-12-14T07:14:40Z |
| format | Article |
| id | doaj.art-894e7c9277494a01bebc685942900d8f |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-14T07:14:40Z |
| publishDate | 2018-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-894e7c9277494a01bebc685942900d8f2022-12-21T23:11:44ZengAmerican Society for MicrobiologymSphere2379-50422018-02-013110.1128/mSphere.00586-17Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory ResponseYongjin Liu0Steven Kyle1Paul D. Straight2Biochemistry and Biophysics Department, Texas A&M University, College Station, Texas, USABiochemistry and Biophysics Department, Texas A&M University, College Station, Texas, USABiochemistry and Biophysics Department, Texas A&M University, College Station, Texas, USAABSTRACT Competitive interactions between bacteria reveal physiological adaptations that benefit fitness. Bacillus subtilis is a Gram-positive species with several adaptive mechanisms for competition and environmental stress. Biofilm formation, sporulation, and motility are the outcomes of widespread changes in a population of B. subtilis. These changes emerge from complex, regulated pathways for adapting to external stresses, including competition from other species. To identify competition-specific functions, we cultured B. subtilis with multiple species of Streptomyces and observed altered patterns of growth for each organism. In particular, when plated on agar medium near Streptomyces venezuelae, B. subtilis initiates a robust and reproducible mobile response. To investigate the mechanistic basis for the interaction, we determined the type of motility used by B. subtilis and isolated inducing metabolites produced by S. venezuelae. Bacillus subtilis has three defined forms of motility: swimming, swarming, and sliding. Streptomyces venezuelae induced sliding motility specifically in our experiments. The inducing agents produced by S. venezuelae were identified as chloramphenicol and a brominated derivative at subinhibitory concentrations. Upon further characterization of the mobile response, our results demonstrated that subinhibitory concentrations of chloramphenicol, erythromycin, tetracycline, and spectinomycin all activate a sliding motility response by B. subtilis. Our data are consistent with sliding motility initiating under conditions of protein translation stress. This report underscores the importance of hormesis as an early warning system for potential bacterial competitors and antibiotic exposure. IMPORTANCE Antibiotic resistance is a major challenge for the effective treatment of infectious diseases. Identifying adaptive mechanisms that bacteria use to survive low levels of antibiotic stress is important for understanding pathways to antibiotic resistance. Furthermore, little is known about the effects of individual bacterial interactions on multispecies communities. This work demonstrates that subinhibitory amounts of some antibiotics produced by streptomycetes induce active motility in B. subtilis, which may alter species interaction dynamics among species-diverse bacterial communities in natural environments. The use of antibiotics at subinhibitory concentrations results in many changes in bacteria, including changes in biofilm formation, small-colony variants, formation of persisters, and motility. Identifying the mechanistic bases of these adaptations is crucial for understanding how bacterial communities are impacted by antibiotics.https://journals.asm.org/doi/10.1128/mSphere.00586-17Bacillus subtilisStreptomyces venezuelaeantibioticschloramphenicolcompetitionhormesis |
| spellingShingle | Yongjin Liu Steven Kyle Paul D. Straight Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response mSphere Bacillus subtilis Streptomyces venezuelae antibiotics chloramphenicol competition hormesis |
| title | Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response |
| title_full | Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response |
| title_fullStr | Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response |
| title_full_unstemmed | Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response |
| title_short | Antibiotic Stimulation of a <named-content content-type="genus-species">Bacillus subtilis</named-content> Migratory Response |
| title_sort | antibiotic stimulation of a named content content type genus species bacillus subtilis named content migratory response |
| topic | Bacillus subtilis Streptomyces venezuelae antibiotics chloramphenicol competition hormesis |
| url | https://journals.asm.org/doi/10.1128/mSphere.00586-17 |
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