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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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The switch from rods to cocci. (A and B) Low (A) and high (B) magnifications of a competing colony. (C) Colonies formed from a single bacterium taken from zone 9 (rods) and from zone 2 (cocci). (D) Transmission electron microscopy of P. dendritiformis rod-shaped, motile cells (left). Cocci (cross-section image) are shown at the same magnification as are the rods (middle panel) and at a higher magnification, revealing incipient cell division (right). (E) The number of bacteria recovered from each zone (250- by 250-µm area) indicated in panels A and B. No bacteria were recovered from zone 1, and only cocci grew from zone 2. The proportion of rod-shaped bacteria increased with increasing distance from the inhibited interface, and only rods were recovered from zones 8 and 9.
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f1: The switch from rods to cocci. (A and B) Low (A) and high (B) magnifications of a competing colony. (C) Colonies formed from a single bacterium taken from zone 9 (rods) and from zone 2 (cocci). (D) Transmission electron microscopy of P. dendritiformis rod-shaped, motile cells (left). Cocci (cross-section image) are shown at the same magnification as are the rods (middle panel) and at a higher magnification, revealing incipient cell division (right). (E) The number of bacteria recovered from each zone (250- by 250-µm area) indicated in panels A and B. No bacteria were recovered from zone 1, and only cocci grew from zone 2. The proportion of rod-shaped bacteria increased with increasing distance from the inhibited interface, and only rods were recovered from zones 8 and 9.

Mentions: To examine the survival of P. dendritiformis during colonial competition, we inoculated two colonies onto low-nutrient peptone agar and allowed them to grow at 30°C until inhibition and killing of bacteria by Slf at the interface were evident (Fig. 1A and 1B, zone 1). Microscopy of cells within the zone of inhibition (Fig. 1A and 1B, zones 2 to 7) revealed the presence of small (0.7-µm-diameter) vegetative cocci that lack flagella (Fig. 1C and 1D). Comparison of the DNA sequences of the 16S rRNA genes of the cocci and rods showed that they were identical, ruling out contaminants (data not shown). Only cocci were recovered from the area closest to the competing colony (Fig. 1A and 1B, zone 2). No spores were seen in the zone of inhibition or in zones 2 and 3 (spore observation was done as previously described [11]). The proportion of rods increased with increasing distance from the competing colony (Fig. 1E). The correlation between proximity to the competing colony and proportion of cocci suggested that their presence was related to the concentration of the lethal factor Slf (11). To test this, we placed purified Slf next to a single growing colony, producing a zone of killing (Fig. 2A). Colonies of cocci could be seen in the inhibited region (Fig. 2A to 2C, zones 2 to 7) after approximately 2 weeks. No spores were observed in zones 1 to 3, where only cocci were found, and few spores were observed in zones 4 and 5. Spore density in zones 6 and 7 was the same as that in colonies not exposed to Slf (see Fig. S5 in reference 11).


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)

The switch from rods to cocci. (A and B) Low (A) and high (B) magnifications of a competing colony. (C) Colonies formed from a single bacterium taken from zone 9 (rods) and from zone 2 (cocci). (D) Transmission electron microscopy of P. dendritiformis rod-shaped, motile cells (left). Cocci (cross-section image) are shown at the same magnification as are the rods (middle panel) and at a higher magnification, revealing incipient cell division (right). (E) The number of bacteria recovered from each zone (250- by 250-µm area) indicated in panels A and B. No bacteria were recovered from zone 1, and only cocci grew from zone 2. The proportion of rod-shaped bacteria increased with increasing distance from the inhibited interface, and only rods were recovered from zones 8 and 9.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f1: The switch from rods to cocci. (A and B) Low (A) and high (B) magnifications of a competing colony. (C) Colonies formed from a single bacterium taken from zone 9 (rods) and from zone 2 (cocci). (D) Transmission electron microscopy of P. dendritiformis rod-shaped, motile cells (left). Cocci (cross-section image) are shown at the same magnification as are the rods (middle panel) and at a higher magnification, revealing incipient cell division (right). (E) The number of bacteria recovered from each zone (250- by 250-µm area) indicated in panels A and B. No bacteria were recovered from zone 1, and only cocci grew from zone 2. The proportion of rod-shaped bacteria increased with increasing distance from the inhibited interface, and only rods were recovered from zones 8 and 9.
Mentions: To examine the survival of P. dendritiformis during colonial competition, we inoculated two colonies onto low-nutrient peptone agar and allowed them to grow at 30°C until inhibition and killing of bacteria by Slf at the interface were evident (Fig. 1A and 1B, zone 1). Microscopy of cells within the zone of inhibition (Fig. 1A and 1B, zones 2 to 7) revealed the presence of small (0.7-µm-diameter) vegetative cocci that lack flagella (Fig. 1C and 1D). Comparison of the DNA sequences of the 16S rRNA genes of the cocci and rods showed that they were identical, ruling out contaminants (data not shown). Only cocci were recovered from the area closest to the competing colony (Fig. 1A and 1B, zone 2). No spores were seen in the zone of inhibition or in zones 2 and 3 (spore observation was done as previously described [11]). The proportion of rods increased with increasing distance from the competing colony (Fig. 1E). The correlation between proximity to the competing colony and proportion of cocci suggested that their presence was related to the concentration of the lethal factor Slf (11). To test this, we placed purified Slf next to a single growing colony, producing a zone of killing (Fig. 2A). Colonies of cocci could be seen in the inhibited region (Fig. 2A to 2C, zones 2 to 7) after approximately 2 weeks. No spores were observed in zones 1 to 3, where only cocci were found, and few spores were observed in zones 4 and 5. Spore density in zones 6 and 7 was the same as that in colonies not exposed to Slf (see Fig. S5 in reference 11).

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