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Metabolic co-dependence gives rise to collective oscillations within biofilms.

Liu J, Prindle A, Humphries J, Gabalda-Sagarra M, Asally M, Lee DY, Ly S, Garcia-Ojalvo J, Süel GM - Nature (2015)

Bottom Line: It remains unclear how these opposing interactions are resolved at the population level.We discover that this conflict between protection and starvation is resolved through emergence of long-range metabolic co-dependence between peripheral and interior cells.As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells.

View Article: PubMed Central - PubMed

Affiliation: Division of Biological Sciences, University of California San Diego, California 92093, USA.

ABSTRACT
Cells that reside within a community can cooperate and also compete with each other for resources. It remains unclear how these opposing interactions are resolved at the population level. Here we investigate such an internal conflict within a microbial (Bacillus subtilis) biofilm community: cells in the biofilm periphery not only protect interior cells from external attack but also starve them through nutrient consumption. We discover that this conflict between protection and starvation is resolved through emergence of long-range metabolic co-dependence between peripheral and interior cells. As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells. We show that this collective oscillation in biofilm growth benefits the community in the event of a chemical attack. These findings indicate that oscillations support population-level conflict resolution by coordinating competing metabolic demands in space and time, suggesting new strategies to control biofilm growth.

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Related in: MedlinePlus

Growth rate oscillations persist in various mutant strains. a, opp operon deletion (deficient in quorum sensing). b, comX deletion (deficient in quorum sensing). c, tapA operon deletion (extracellular matrix component deletion). d, tapA operon overexpression (Phyperspank-tapA operon, 1mM IPTG). e, hag deletion (deficient in swimming and swarming). These results show that the corresponding genes and processes are not required for biofilm oscillations.
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Figure 14: Growth rate oscillations persist in various mutant strains. a, opp operon deletion (deficient in quorum sensing). b, comX deletion (deficient in quorum sensing). c, tapA operon deletion (extracellular matrix component deletion). d, tapA operon overexpression (Phyperspank-tapA operon, 1mM IPTG). e, hag deletion (deficient in swimming and swarming). These results show that the corresponding genes and processes are not required for biofilm oscillations.

Mentions: The intriguing discovery of biofilm oscillations presented here also provokes new questions. While cellular processes such as swarming or expression of extracellular matrix components are not required for the observed biofilm oscillations (Extended Data Fig. 10), it will be interesting to pursue whether such cellular processes are influenced by oscillatory dynamics29. Another question worth pursuing is whether metabolic codependence can also arise in other biofilm-forming species. Perhaps other metabolic branches where metabolites can be shared among cells could also give rise to oscillations in biofilm growth. It will be exciting to pursue these questions in future studies to obtain a better understanding of biofilm development.


Metabolic co-dependence gives rise to collective oscillations within biofilms.

Liu J, Prindle A, Humphries J, Gabalda-Sagarra M, Asally M, Lee DY, Ly S, Garcia-Ojalvo J, Süel GM - Nature (2015)

Growth rate oscillations persist in various mutant strains. a, opp operon deletion (deficient in quorum sensing). b, comX deletion (deficient in quorum sensing). c, tapA operon deletion (extracellular matrix component deletion). d, tapA operon overexpression (Phyperspank-tapA operon, 1mM IPTG). e, hag deletion (deficient in swimming and swarming). These results show that the corresponding genes and processes are not required for biofilm oscillations.
© Copyright Policy - permissions-link
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4862617&req=5

Figure 14: Growth rate oscillations persist in various mutant strains. a, opp operon deletion (deficient in quorum sensing). b, comX deletion (deficient in quorum sensing). c, tapA operon deletion (extracellular matrix component deletion). d, tapA operon overexpression (Phyperspank-tapA operon, 1mM IPTG). e, hag deletion (deficient in swimming and swarming). These results show that the corresponding genes and processes are not required for biofilm oscillations.
Mentions: The intriguing discovery of biofilm oscillations presented here also provokes new questions. While cellular processes such as swarming or expression of extracellular matrix components are not required for the observed biofilm oscillations (Extended Data Fig. 10), it will be interesting to pursue whether such cellular processes are influenced by oscillatory dynamics29. Another question worth pursuing is whether metabolic codependence can also arise in other biofilm-forming species. Perhaps other metabolic branches where metabolites can be shared among cells could also give rise to oscillations in biofilm growth. It will be exciting to pursue these questions in future studies to obtain a better understanding of biofilm development.

Bottom Line: It remains unclear how these opposing interactions are resolved at the population level.We discover that this conflict between protection and starvation is resolved through emergence of long-range metabolic co-dependence between peripheral and interior cells.As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells.

View Article: PubMed Central - PubMed

Affiliation: Division of Biological Sciences, University of California San Diego, California 92093, USA.

ABSTRACT
Cells that reside within a community can cooperate and also compete with each other for resources. It remains unclear how these opposing interactions are resolved at the population level. Here we investigate such an internal conflict within a microbial (Bacillus subtilis) biofilm community: cells in the biofilm periphery not only protect interior cells from external attack but also starve them through nutrient consumption. We discover that this conflict between protection and starvation is resolved through emergence of long-range metabolic co-dependence between peripheral and interior cells. As a result, biofilm growth halts periodically, increasing nutrient availability for the sheltered interior cells. We show that this collective oscillation in biofilm growth benefits the community in the event of a chemical attack. These findings indicate that oscillations support population-level conflict resolution by coordinating competing metabolic demands in space and time, suggesting new strategies to control biofilm growth.

Show MeSH
Related in: MedlinePlus