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Surviving bacterial sibling rivalry: inducible and reversible phenotypic switching in Paenibacillus dendritiformis.

Be'er A, Florin EL, Fisher CR, Swinney HL, Payne SM - MBio (2011)

Bottom Line: When competing with sibling colonies, Paenibacillus dendritiformis produces a lethal protein (Slf) that kills cells at the interface of encroaching colonies.Slf also induces a small proportion of the cells to switch from motile, rod-shaped cells to nonmotile, Slf-resistant, vegetative cocci.Genes encoding components of this phenotypic switching pathway are widespread among bacterial species, suggesting that this survival mechanism is not unique to P. dendritiformis.

View Article: PubMed Central - PubMed

Affiliation: Center for Nonlinear Dynamics and Department of Physics, University of Texas at Austin, Austin, Texas, USA.

ABSTRACT

Unlabelled: Natural habitats vary in available nutrients and room for bacteria to grow, but successful colonization can lead to overcrowding and stress. Here we show that competing sibling colonies of Paenibacillus dendritiformis bacteria survive overcrowding by switching between two distinct vegetative phenotypes, motile rods and immotile cocci. Growing colonies of the rod-shaped bacteria produce a toxic protein, Slf, which kills cells of encroaching sibling colonies. However, sublethal concentrations of Slf induce some of the rods to switch to Slf-resistant cocci, which have distinct metabolic and resistance profiles, including resistance to cell wall antibiotics. Unlike dormant spores of P. dendritiformis, the cocci replicate. If cocci encounter conditions that favor rods, they secrete a signaling molecule that induces a switch to rods. Thus, in contrast to persister cells, P. dendritiformis bacteria adapt to changing environmental conditions by inducible and reversible phenotypic switching.

Importance: In favorable environments, species may face space and nutrient limits due to overcrowding. Bacteria provide an excellent model for analyzing principles underlying overcrowding and regulation of density in nature, since their population dynamics can be easily and accurately assessed under controlled conditions. We describe a newly discovered mechanism for survival of a bacterial population during overcrowding. When competing with sibling colonies, Paenibacillus dendritiformis produces a lethal protein (Slf) that kills cells at the interface of encroaching colonies. Slf also induces a small proportion of the cells to switch from motile, rod-shaped cells to nonmotile, Slf-resistant, vegetative cocci. When crowding is reduced and nutrients are no longer limiting, the bacteria produce a signal that induces cocci to switch back to motile rods, allowing the population to spread. Genes encoding components of this phenotypic switching pathway are widespread among bacterial species, suggesting that this survival mechanism is not unique to P. dendritiformis.

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Rod-inducing signal (Ris). (A) Six colonies in close proximity show switching of cocci to rods sooner than does one or two colonies. Numbers indicate the number of colonies in a spot. (B) The time required for switch from cocci to rods depends on the number of coccus colonies in close proximity (as in panel A). Error bars are the standard deviations for 10 cases. (C) The time required for the switch to rods is proportional to the distance between two colonies. (D and E) Addition of Ris causes a single coccus to switch to a rod. (F) Circuit model showing the transitions between various cell forms of P. dendritiformis.
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f5: Rod-inducing signal (Ris). (A) Six colonies in close proximity show switching of cocci to rods sooner than does one or two colonies. Numbers indicate the number of colonies in a spot. (B) The time required for switch from cocci to rods depends on the number of coccus colonies in close proximity (as in panel A). Error bars are the standard deviations for 10 cases. (C) The time required for the switch to rods is proportional to the distance between two colonies. (D and E) Addition of Ris causes a single coccus to switch to a rod. (F) Circuit model showing the transitions between various cell forms of P. dendritiformis.

Mentions: When multiple colonies were present within a spot on the plate, the length of time required for cocci in each colony to switch to rods was proportional to the number of colonies initially present in the spot (Fig. 5A and 5B) and to the proximity of colonies to each other (Fig. 5C). This suggests that the switch is not random but requires a secreted signal which is present in a larger quantity when there are more colonies and diffuses more rapidly when colonies are closer to each other. Such a signaling molecule should be present in culture supernatants. To test for the presence of a secreted inducing signal, cocci were grown in LB broth for 18 h at 30°C, and sterile supernatant from this culture was added to an equal volume of fresh medium prior to inoculation with cocci. In this culture, the switch to rods began at 18 h, whereas switching did not occur in the absence of supernatant until 22 h. This supports the hypothesis that a secreted factor, designated Ris (rod-inducing signal), induces the switch from cocci to rods. Rods grown in rich medium (LB) were also assessed for Ris production. Addition of rod supernatant to a culture of cocci, as described for the coccus supernatant, also induced switching from cocci to rods by 18 h but triggered the switch to the rod phenotype among more than 50% of the population by 18 h, compared to 3% in the culture treated with coccus supernatant. The simplest explanation is that Ris is secreted in greater amounts by the rods. Thus, there may be a positive-feedback loop: cells that switch to the rod phenotype secrete the inducer in larger amounts, accelerating the process of switching among the remaining cocci and ensuring that the transition is complete.


Surviving bacterial sibling rivalry: inducible and reversible phenotypic switching in Paenibacillus dendritiformis.

Be'er A, Florin EL, Fisher CR, Swinney HL, Payne SM - MBio (2011)

Rod-inducing signal (Ris). (A) Six colonies in close proximity show switching of cocci to rods sooner than does one or two colonies. Numbers indicate the number of colonies in a spot. (B) The time required for switch from cocci to rods depends on the number of coccus colonies in close proximity (as in panel A). Error bars are the standard deviations for 10 cases. (C) The time required for the switch to rods is proportional to the distance between two colonies. (D and E) Addition of Ris causes a single coccus to switch to a rod. (F) Circuit model showing the transitions between various cell forms of P. dendritiformis.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3104493&req=5

f5: Rod-inducing signal (Ris). (A) Six colonies in close proximity show switching of cocci to rods sooner than does one or two colonies. Numbers indicate the number of colonies in a spot. (B) The time required for switch from cocci to rods depends on the number of coccus colonies in close proximity (as in panel A). Error bars are the standard deviations for 10 cases. (C) The time required for the switch to rods is proportional to the distance between two colonies. (D and E) Addition of Ris causes a single coccus to switch to a rod. (F) Circuit model showing the transitions between various cell forms of P. dendritiformis.
Mentions: When multiple colonies were present within a spot on the plate, the length of time required for cocci in each colony to switch to rods was proportional to the number of colonies initially present in the spot (Fig. 5A and 5B) and to the proximity of colonies to each other (Fig. 5C). This suggests that the switch is not random but requires a secreted signal which is present in a larger quantity when there are more colonies and diffuses more rapidly when colonies are closer to each other. Such a signaling molecule should be present in culture supernatants. To test for the presence of a secreted inducing signal, cocci were grown in LB broth for 18 h at 30°C, and sterile supernatant from this culture was added to an equal volume of fresh medium prior to inoculation with cocci. In this culture, the switch to rods began at 18 h, whereas switching did not occur in the absence of supernatant until 22 h. This supports the hypothesis that a secreted factor, designated Ris (rod-inducing signal), induces the switch from cocci to rods. Rods grown in rich medium (LB) were also assessed for Ris production. Addition of rod supernatant to a culture of cocci, as described for the coccus supernatant, also induced switching from cocci to rods by 18 h but triggered the switch to the rod phenotype among more than 50% of the population by 18 h, compared to 3% in the culture treated with coccus supernatant. The simplest explanation is that Ris is secreted in greater amounts by the rods. Thus, there may be a positive-feedback loop: cells that switch to the rod phenotype secrete the inducer in larger amounts, accelerating the process of switching among the remaining cocci and ensuring that the transition is complete.

Bottom Line: When competing with sibling colonies, Paenibacillus dendritiformis produces a lethal protein (Slf) that kills cells at the interface of encroaching colonies.Slf also induces a small proportion of the cells to switch from motile, rod-shaped cells to nonmotile, Slf-resistant, vegetative cocci.Genes encoding components of this phenotypic switching pathway are widespread among bacterial species, suggesting that this survival mechanism is not unique to P. dendritiformis.

View Article: PubMed Central - PubMed

Affiliation: Center for Nonlinear Dynamics and Department of Physics, University of Texas at Austin, Austin, Texas, USA.

ABSTRACT

Unlabelled: Natural habitats vary in available nutrients and room for bacteria to grow, but successful colonization can lead to overcrowding and stress. Here we show that competing sibling colonies of Paenibacillus dendritiformis bacteria survive overcrowding by switching between two distinct vegetative phenotypes, motile rods and immotile cocci. Growing colonies of the rod-shaped bacteria produce a toxic protein, Slf, which kills cells of encroaching sibling colonies. However, sublethal concentrations of Slf induce some of the rods to switch to Slf-resistant cocci, which have distinct metabolic and resistance profiles, including resistance to cell wall antibiotics. Unlike dormant spores of P. dendritiformis, the cocci replicate. If cocci encounter conditions that favor rods, they secrete a signaling molecule that induces a switch to rods. Thus, in contrast to persister cells, P. dendritiformis bacteria adapt to changing environmental conditions by inducible and reversible phenotypic switching.

Importance: In favorable environments, species may face space and nutrient limits due to overcrowding. Bacteria provide an excellent model for analyzing principles underlying overcrowding and regulation of density in nature, since their population dynamics can be easily and accurately assessed under controlled conditions. We describe a newly discovered mechanism for survival of a bacterial population during overcrowding. When competing with sibling colonies, Paenibacillus dendritiformis produces a lethal protein (Slf) that kills cells at the interface of encroaching colonies. Slf also induces a small proportion of the cells to switch from motile, rod-shaped cells to nonmotile, Slf-resistant, vegetative cocci. When crowding is reduced and nutrients are no longer limiting, the bacteria produce a signal that induces cocci to switch back to motile rods, allowing the population to spread. Genes encoding components of this phenotypic switching pathway are widespread among bacterial species, suggesting that this survival mechanism is not unique to P. dendritiformis.

Show MeSH
Related in: MedlinePlus