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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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Related in: MedlinePlus

Growth of P. dendritiformis rods and cocci under different conditions. Rods and cocci were cultured separately. (A) Growth of rods and cocci in LB broth at 30°C with aeration. (B) Density of cultures of rods and cocci after 18 h of growth under different conditions. Rich medium, LB broth; defined medium, RDM. Error bars are the standard deviations for 10 cases.
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f3: Growth of P. dendritiformis rods and cocci under different conditions. Rods and cocci were cultured separately. (A) Growth of rods and cocci in LB broth at 30°C with aeration. (B) Density of cultures of rods and cocci after 18 h of growth under different conditions. Rich medium, LB broth; defined medium, RDM. Error bars are the standard deviations for 10 cases.

Mentions: To determine differences between the two phenotypes, the growth and metabolism of cocci and rods under different conditions were compared. Cocci and rods were restreaked multiple times for isolation and maintained as separate stocks. Cocci and rods produced pure cultures in rich (LB) broth and grew at the same rates during exponential phase (Fig. 3A). At 30°C in LB broth, cocci reached a higher density than did the rods, but the rods grew to higher density at 37°C. The rods also outgrew the cocci in chemically defined medium (rich defined medium [RDM] [13]) (Fig. 3B). Addition of purified Slf to cultures confirmed that cocci but not rods were resistant to killing by Slf (Fig. 3B). A more detailed metabolic profiling using Biolog Phenotype MicroArrays (see Fig. S1 in the supplemental material) showed differences in carbon, nitrogen, phosphorus, and sulfur source utilization and in resistance to environmental stresses and antibiotics. In particular, cocci were much more resistant than rods were to osmotic stress and penicillins, indicating differences in cell wall and perhaps membrane structures. Thus, the cocci and rods exhibited striking differences in their abilities to survive and replicate under certain environmental and nutrient conditions.


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)

Growth of P. dendritiformis rods and cocci under different conditions. Rods and cocci were cultured separately. (A) Growth of rods and cocci in LB broth at 30°C with aeration. (B) Density of cultures of rods and cocci after 18 h of growth under different conditions. Rich medium, LB broth; defined medium, RDM. Error bars are the standard deviations for 10 cases.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: Growth of P. dendritiformis rods and cocci under different conditions. Rods and cocci were cultured separately. (A) Growth of rods and cocci in LB broth at 30°C with aeration. (B) Density of cultures of rods and cocci after 18 h of growth under different conditions. Rich medium, LB broth; defined medium, RDM. Error bars are the standard deviations for 10 cases.
Mentions: To determine differences between the two phenotypes, the growth and metabolism of cocci and rods under different conditions were compared. Cocci and rods were restreaked multiple times for isolation and maintained as separate stocks. Cocci and rods produced pure cultures in rich (LB) broth and grew at the same rates during exponential phase (Fig. 3A). At 30°C in LB broth, cocci reached a higher density than did the rods, but the rods grew to higher density at 37°C. The rods also outgrew the cocci in chemically defined medium (rich defined medium [RDM] [13]) (Fig. 3B). Addition of purified Slf to cultures confirmed that cocci but not rods were resistant to killing by Slf (Fig. 3B). A more detailed metabolic profiling using Biolog Phenotype MicroArrays (see Fig. S1 in the supplemental material) showed differences in carbon, nitrogen, phosphorus, and sulfur source utilization and in resistance to environmental stresses and antibiotics. In particular, cocci were much more resistant than rods were to osmotic stress and penicillins, indicating differences in cell wall and perhaps membrane structures. Thus, the cocci and rods exhibited striking differences in their abilities to survive and replicate under certain environmental and nutrient conditions.

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