ABSTRACT 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. 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.
[1]
E. Ben-Jacob,et al.
Lethal protein produced in response to competition between sibling bacterial colonies
,
2010,
Proceedings of the National Academy of Sciences.
[2]
R. Dobler,et al.
Kin-selected siblicide and cannibalism in the European earwig
,
2010
.
[3]
H. Swinney,et al.
Paenibacillus dendritiformis Bacterial Colony Growth Depends on Surfactant but Not on Bacterial Motion
,
2009,
Journal of bacteriology.
[4]
Eshel Ben-Jacob,et al.
Deadly competition between sibling bacterial colonies
,
2009,
Proceedings of the National Academy of Sciences.
[5]
E. Greenberg,et al.
Genetic Determinants of Self Identity and Social Recognition in Bacteria
,
2008,
Science.
[6]
R. Rothstein,et al.
Genome-Wide Analysis of Rad52 Foci Reveals Diverse Mechanisms Impacting Recombination
,
2007,
PLoS genetics.
[7]
Jean-Pierre Claverys,et al.
Cannibalism and fratricide: mechanisms and raisons d'être
,
2007,
Nature Reviews Microbiology.
[8]
K. Young.
The Selective Value of Bacterial Shape
,
2006,
Microbiology and Molecular Biology Reviews.
[9]
S. Leibler,et al.
Bacterial Persistence as a Phenotypic Switch
,
2004,
Science.
[10]
J. Errington.
Regulation of endospore formation in Bacillus subtilis
,
2003,
Nature Reviews Microbiology.
[11]
R. Losick,et al.
Cannibalism by Sporulating Bacteria
,
2003,
Science.
[12]
G. Belovsky,et al.
Experimental studies of extinction dynamics
,
1999,
Science.
[13]
C. Lämmler,et al.
Studies on the rod-coccus life cycle of Rhodococcus equi.
,
1997,
Zentralblatt fur Veterinarmedizin. Reihe B. Journal of veterinary medicine. Series B.
[14]
J. Costerton,et al.
Digital image analysis of growth and starvation responses of a surface-colonizing Acinetobacter sp
,
1995,
Journal of bacteriology.
[15]
R. Hengge-aronis,et al.
Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S
,
1991,
Journal of bacteriology.
[16]
F. V. vom Saal,et al.
The regulation of infanticide and parental behavior: implications for reproductive success in male mice.
,
1982,
Science.
[17]
B. Lister.
Resource variation and the structure of British bird communities.
,
1980,
Proceedings of the National Academy of Sciences of the United States of America.
[18]
F. Neidhardt,et al.
Culture Medium for Enterobacteria
,
1974,
Journal of bacteriology.
[19]
T. Gray,et al.
Characteristics of Arthrobacter Grown in Continuous Culture
,
1974
.
[20]
J. Maclear.
Captain Maclear's Observations
,
1872,
Nature.
[21]
E Ben-Jacob,et al.
Cooperative organization of bacterial colonies: from genotype to morphotype.
,
1998,
Annual review of microbiology.