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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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P. dendritiformis switch from cocci to rods. Low (A, C, and E)- and high (B, D, and F)-resolution pictures of a colony grown from a single coccus on LB agar. The colony contains only cocci 48 h after inoculation (A and B). At 50 h (C and D), rods, swimming individually, appear at the colony edge. Four hours later (E and F), the rods are swarming. Rods appeared nearly simultaneously (within ~10 min) at multiple locations along the edge of the same colony and other colonies grown on the same plate.
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f4: P. dendritiformis switch from cocci to rods. Low (A, C, and E)- and high (B, D, and F)-resolution pictures of a colony grown from a single coccus on LB agar. The colony contains only cocci 48 h after inoculation (A and B). At 50 h (C and D), rods, swimming individually, appear at the colony edge. Four hours later (E and F), the rods are swarming. Rods appeared nearly simultaneously (within ~10 min) at multiple locations along the edge of the same colony and other colonies grown on the same plate.

Mentions: If the switch were an adaptive response to overcrowding, it would be likely that cocci could switch back to the rod morphology under conditions that favor motile rods. Therefore, individual cocci were inoculated on LB swarm plates (1% agar) and observed for the appearance of motile rods. The colonies expanded slowly for the first 48 h, during which time only cocci were detected (Fig. 4A and 4B; see Movie S1 in the supplemental material). After 50 h, rod-shaped, motile bacteria were observed at the edge of the colony (Fig. 4C and 4D; Movie S2), and within 4 h after the initial appearance of rods, the motile rods began to swarm in a thin liquid layer (Fig. 4E and 4F; Movies S3 and S4). The rods multiplied and 2 h later began to swarm in multiple layers, similar to colonies initiated from single rods (Movie S5).


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)

P. dendritiformis switch from cocci to rods. Low (A, C, and E)- and high (B, D, and F)-resolution pictures of a colony grown from a single coccus on LB agar. The colony contains only cocci 48 h after inoculation (A and B). At 50 h (C and D), rods, swimming individually, appear at the colony edge. Four hours later (E and F), the rods are swarming. Rods appeared nearly simultaneously (within ~10 min) at multiple locations along the edge of the same colony and other colonies grown on the same plate.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: P. dendritiformis switch from cocci to rods. Low (A, C, and E)- and high (B, D, and F)-resolution pictures of a colony grown from a single coccus on LB agar. The colony contains only cocci 48 h after inoculation (A and B). At 50 h (C and D), rods, swimming individually, appear at the colony edge. Four hours later (E and F), the rods are swarming. Rods appeared nearly simultaneously (within ~10 min) at multiple locations along the edge of the same colony and other colonies grown on the same plate.
Mentions: If the switch were an adaptive response to overcrowding, it would be likely that cocci could switch back to the rod morphology under conditions that favor motile rods. Therefore, individual cocci were inoculated on LB swarm plates (1% agar) and observed for the appearance of motile rods. The colonies expanded slowly for the first 48 h, during which time only cocci were detected (Fig. 4A and 4B; see Movie S1 in the supplemental material). After 50 h, rod-shaped, motile bacteria were observed at the edge of the colony (Fig. 4C and 4D; Movie S2), and within 4 h after the initial appearance of rods, the motile rods began to swarm in a thin liquid layer (Fig. 4E and 4F; Movies S3 and S4). The rods multiplied and 2 h later began to swarm in multiple layers, similar to colonies initiated from single rods (Movie S5).

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