Abstract
BackgroundThe survival of bacteria largely depends on signaling systems that coordinate cell responses to environmental cues. Previous studies on the two-component ColRS signal system in Pseudomonas putida revealed a peculiar subpopulation lysis phenotype of colR mutant that grows on solid glucose medium. Here, we aimed to clarify the reasons for the lysis of bacteria.ResultsWe present evidence that the lysis defect of P. putida colR mutant is linked to hunger response. A subpopulation prone to lysis was located in the periphery of bacterial cultures growing on solid medium. Cell lysis was observed in glucose-limiting, but not in glucose-rich conditions. Furthermore, lysis was also alleviated by exhaustion of glucose from the medium which was evidenced by a lower lysis of central cells compared to peripheral ones. Thus, lysis takes place at a certain glucose concentration range that most probably provides bacteria a hunger signal. An analysis of membrane protein pattern revealed several hunger-induced changes in the bacterial outer membrane: at glucose limitation the amount of OprB1 channel protein was significantly increased whereas that of OprE was decreased. Hunger-induced up-regulation of OprB1 correlated in space and time with the lysis of the colR mutant, indicating that hunger response is detrimental to the colR-deficient bacteria. The amount of OprB1 is controlled post-transcriptionally and derepression of OprB1 in glucose-limiting medium depends at least partly on the carbon catabolite regulator protein Crc. The essentiality of ColR in hunger response can be bypassed by reducing the amount of certain outer membrane proteins. In addition to depletion of OprB1, the lysis defect of colR mutant can be suppressed by the down-regulation of OprF levels and the hindering of SecB-dependent protein secretion.ConclusionsWe show that Pseudomonas putida growing on solid glucose medium adapts to glucose limitation through up-regulation of the sugar channel protein OprB1 that probably allows enhanced acquisition of a limiting nutrient. However, to survive such hunger response bacteria need signalling by the ColRS system. Hence, the ColRS system should be considered a safety factor in hunger response that ensures the welfare of the cell membrane during the increased expression of certain membrane proteins.
Highlights
The survival of bacteria largely depends on signaling systems that coordinate cell responses to environmental cues
Glucose-specific lysis of the colR mutant occurs only on solid medium and increases in time To specify the requirements for the glucose-related lysis of the colR-deficient P. putida, cell lysis was measured at different time points of growth both on solid and in liquid media with either glucose or gluconate as a carbon source
In good accordance with our previous results, colR-dependent lysis did not occur on gluconate medium [25]. These data suggest that ColRS system is important for P. putida that grows on glucose solid medium
Summary
The survival of bacteria largely depends on signaling systems that coordinate cell responses to environmental cues. Most bacteria live in constantly changing and often nutritionally limiting environments. The success of bacteria in such conditions depends on their ability to sense the nutritional status of the environment and respond appropriately by reprogramming their gene expression and cell metabolism. Nutrient depletion triggers starvation response that involves the stress-specific sigma factor RpoS and results in drastic changes in gene expression and arrests cell nutrient [2,4]. As the rpoS gene was not induced in these conditions, hunger-induced changes should be considered distinct from stationary phase response [8]. The mutants that are defective in some hunger-induced transporter have reduced fitness in nutrient-poor conditions [5,9]
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