Abstract
Quorum sensing (QS) is a cell density-dependent mechanism which enables a population of bacteria to coordinate cooperative behaviors in response to the accumulation of self-produced autoinducer signals in their local environment. An emerging framework is that the adaptive significance of QS in the regulation of production of costly extracellular metabolites (“public goods”) is to maintain the homeostasis of cooperation. We investigated this model using the phytopathogenic bacterium Burkholderia glumae, which we have previously demonstrated uses QS to regulate the production of rhamnolipids, extracellular surface-active glycolipids promoting the social behavior called “swarming motility.” Using mass spectrometric quantification and chromosomal lux-based gene expression, we made the unexpected finding that when unrestricted nutrient resources are provided, production of rhamnolipids is carried out completely independently of QS regulation. This is a unique observation among known QS-controlled factors in bacteria. On the other hand, under nutrient-limited conditions, QS then becomes the main regulating mechanism, significantly enhancing the specific rhamnolipids yield. Accordingly, decreasing nutrient concentrations amplifies rhamnolipid biosynthesis gene expression, revealing a system where QS-dependent regulation is specifically triggered by the growth rate of the population, rather than by its cell density. Furthermore, a gradual increase in QS signal specific concentration upon decrease of specific growth rate suggests a reduction in quorum threshold, which reflects an increase in cellular demand for production of QS-dependent target gene product at low density populations. Integration of growth rate with QS as a decision-making mechanism for biosynthesis of costly metabolites, such as rhamnolipids, could serve to assess the demand and timing for expanding the carrying capacity of a population through spatial expansion mechanisms, such as swarming motility, thus promoting the chances of survival, even if the cell density might not be high enough for an otherwise efficient production of rhamnolipids. In conclusion, we propose that the adaptive significance of growth rate-dependent functionality of QS in biosynthesis of costly public goods lies within providing a regulatory mechanism for selecting the optimal trade-off between survival and efficiency.
Highlights
Quorum sensing (QS) is a cell density-dependent mechanism which enables a population of bacteria to synchronize the expression of behaviors in response to the accumulation of self-produced autoinducer signals in their local environment (Fuqua et al, 1994)
We found that growth rate, and not cell density itself, is the key factor triggering the QS-dependent regulation of rhamnolipid biosynthesis
To strengthen our understanding on the specific role of QS regulation in the production of rhamnolipids in B. glumae we studied the kinetics of rhamnolipid production in wild-type strain and tofI− mutant using a minimal [mineral salts medium (MSM)] typically used to promote production of rhamnolipids and a complex nutrient broth (NB) culture media, both supplemented with nonlimiting glycerol as carbon source ( MSMG and NBG)
Summary
Quorum sensing (QS) is a cell density-dependent mechanism which enables a population of bacteria to synchronize the expression of behaviors in response to the accumulation of self-produced autoinducer signals in their local environment (Fuqua et al, 1994) Such auto-induction regulatory systems are implicated in regulation of various cooperative phenotypes ranging from bioluminescence, virulence and nutrient acquisition to multicellular swarming motility and biofilm development (Bainton et al, 1992; Passador et al, 1993; Stevens and Greenberg, 1997; Davies et al, 1998; Daniels et al, 2004; An et al, 2014). Another possible solution to stabilizing cooperation is ‘policing,’ where cooperators actively penalize social cheats to hinder their success (Wang et al, 2015)
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