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It has long been known that some groups of bacteria exhibit complex patterns of coordinated behavior and that in several cases, the behaviors of these populations of cells are regulated by diffusible chemical signals. These behaviors include biolu- minescence, the horizontal transfer of DNA, the formation of biofilms, and the production of pathogenesis factors, antibiot- ics, and other secondary metabolites (32). A broad variety of signal molecules and signal receptors have been identified over the past 20 years. Of these, possibly the most intriguing signal consists of a molecule called autoinducer 2 (AI-2), which is made by a wide variety of bacteria. The discovery of AI-2, by Bonnie Bassler and her colleagues at Princeton University, sent shock waves through the scientific community, since their discoveries suggested, first, that virtually all bacteria might send and receive chemical signals, and second, that these bac- teria might signal intergenerically, using what has been termed a "bacterial Esperanto." What did all these bacteria need to say to each other? AI-2 was first discovered in the marine bioluminescent bacterium Vibrio harveyi, which uses two par- allel signaling pathways to control expression of its lux operon. In this issue, the Bassler group reports that this communication system also regulates expression of a type III secretion (TTS) system, which presumably translocates specific proteins to eu- karyotic host cells (10a). Surprisingly, expression of the TTS system and the lux operon are inversely regulated in that AI-1 and AI-2 repress the former but activate that latter. Most known bacterial signaling systems fall into two classes. Gram-positive bacteria typically communicate using oligopep- tide signals that are detected by two-component phosphorelay pathways (8), while proteobacteria generally signal via acyl- homoserine lactones (AHLs) that are synthesized by proteins that resemble LuxI of Vibrio fischeri and are detected by tran- scription factors that resemble LuxR of V. fischeri. These sys- tems are sometimes referred to as quorum-sensing regulators, which suggests that the purpose of these systems is to estimate population density. It is unfortunate that this term is used so freely, since there is little or no evidence that the purpose of any of these signaling systems is to take a bacterial census. It is just as likely that these systems are designed to coordinate the behavior of cell populations rather than to enumerate them. The signaling system of V. harveyi does not resemble either of the family systems described above. Instead, V. harveyi sig- nals using AI-2 and another chemical signal called AI-1 (1, 2). AI-1 is 3-hydroxy-butanoylhomoserine lactone, which is a member of the family of AHL signals (3). Surprisingly, the AI-1 synthase (LuxM) does not resemble members of the LuxI family, although it is a member of a second small family of synthases that so far has been found only in the genus Vibrio. Detection of AI-1 requires a membrane-spanning two-compo- nent kinase (LuxN), while detection of AI-2 requires a periplasmic protein that resembles the ribose binding protein (LuxP) (2) and a second two-component kinase (LuxQ) (1, 2). Both LuxN and LuxQ are hybrid proteins containing a sensor kinase domain and a response regulator domain that funnel phosphoryl groups via LuxU to LuxO, a 54 -dependent tran- scriptional activator that is hypothesized to control the expres- sion of an unidentified repressor of luxR. LuxR (not related to the V. fischeri LuxR protein) activates the luciferase structural operon (luxCDABE) (2, 9, 16). In the absence of both signals,

journal of bacteriology

Reciprocal Regulation of Bioluminescence and Type III Protein Secretion in <i>Vibrio harveyi</i> and <i>Vibrio parahaemolyticus</i> in Response to Diffusible Chemical Signals

Reciprocal Regulation of Bioluminescence and Type III Protein Secretion in Vibrio harveyi and Vibrio parahaemolyticus in Response to Diffusible Chemical Signals