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Microbial Chatter:
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This eBriefing was written for the New York Academy of Sciences in the Spring of 2006. It can be accessed by members, complete with slides and visuals, at www.nyas.org Bacteria are gregarious by nature; preferring to crowd together in complex, multi-species communities whether on abiotic surfaces or living tissue. They are certainly not the solitary, reclusive cells people once thought they were. Nor are they guileless. Even the most eukaryotically chauvinistic among us have to agree that bacteria are superbly well adapted to lives of infinite uncertainty and intense competition. The ability to communicate and cooperate goes a long way to ensuring their survival. Recently discovered species-specific and universal intracellular signaling molecules reveal that bacteria talk with one another using a rich chemical lexicon. Three of the languages, described in this eBriefing, enable bacteria living together in large groups to keep tabs on each other and coordinate their behavior accordingly; thereby acting very much like a single, multicellular organism. SpeakerBonnie Bassler, Princeton University, Howard Hughes Medical Institute Held at the New York Academy of Sciences | March 15, 2006 Sponsored by the Microbiology Section Reported by Marcia Stone Highlights
The secret language of bacteriaBonnie Bassler of Princeton University and the Howard Hughes Medical Institute spends her professional life eavesdropping on bacteria. She shared some of their secret conversations with a riveted audience at the March 15, 2005 meeting of the New York Academy of Sciences’ Microbiology Section. “We scientists were all wrong thinking that bacteria live asocial, reclusive lives,” said Bassler. “There isn’t any way they could accomplish the terrible and the wonderful things they do on earth as individuals.” Bacteria chatter continuously and their words are chemical, continued Bassler, proving her point by describing some recently translated bacterial languages in a communication system called “quorum sensing,” which consists of the production, release, and subsequent detection of and response to threshold concentrations of small signaling molecules called autoinducers (AIs). An individual bacterium is ineffectual in this system. Quorum sensing exerts an effect only when a message is “voiced” by a large number of cells (i.e., a quorum) in unison. Callout: Bacteria chatter continuously, and their words are chemical. The synchronous response of bacterial populations to autoinducers confers a form of multicellularity to bacteria. Quorum-sensing controlled processes—for example, bioluminescence, biofilm formation, virulence-factor expression, motility, sporulation, mating, and antibiotic production—require the concerted action of many cells. As the population grows, extracellular autoinducer levels increase. Because the concentration of autoinducers in their environment correlates nicely with population density, it gives bacteria a way to “count” one another and, when a critical cell number has been reached, to respond with a population-wide alteration of gene expression. Multilingual microbes“Not only can bacteria talk with one another,” said Bassler, “they’re multilingual.” There are three major quorum-sensing languages: Gram-negative bacteria talk among themselves with acylated homoserine lactone (AHL) autoinducers, whereas Gram-positive cells use oligopeptides. Additionally, most, if not all, well- socialized bacteria appear fluent in autoinducer 2 (AI-2), universal quorum-sensing molecules that seem to be an interspecies language of choice. Callout: “Not only can bacteria talk with one another, they’re multilingual.” That bacteria have a common language should not be unexpected. Most live in mixed-species consortia and probably converse with unrelated microbes more often than anyone ever envisioned. As an example, Bassler noted that there are about 600 species of bacteria on our teeth every morning in exactly the same organization as the night before. The only way they can build these very “beautiful and complicated” biofilms is to know exactly what other cells are out there and use the information to function collectively as a working conglomerate. In brief, Gram-negative bacterial AHLs are synthesized in the cell’s cytoplasm from S-adenosyl methionine (SAM) and pass freely through the cell membrane into the extracellular environment, where they’re available to other organisms. Each species of Gram-negative bacteria produces a unique AHL or unique combination of AHLs. The homoserine lactones portions of these molecules are identical, but each acyl side chain is a little bit different [Slide #4. Acyl-Homoserine Lactone Autoinducers]. Thus, only like-minded bacteria recognize and process any particular AHL signal. Gram-positive bacteria use oligopeptide autoinducers instead of AHLs for species-specific communications. The oligopeptides are actively exported out of the cell, where they interact with the external domains of membrane-bound sensor proteins in receptive bacteria. Specificity exists because each sensor protein is highly selective for any given peptide signal. In contrast to species-specific quorum sensing, a wide variety of bacteria also produce and detect AI-2. The AI-2 synthases, encoded by luxS genes, all produce 4,5-dihydroxy-2,3-pentanedione (DPD) which can rearrange itself spontaneously. A blend of different AI-2 molecules in any given environment yields accurate information on the specific identities of the inhabitants. To date, LuxS enzymes have been identified in more than 55 Gram-negative and Gram-positive bacterial species. You light up my lifeThe idea that bacteria communicate with each other started with two “ridiculous” bacteria: Vibrio fischeri and Vibrio harveyi, marine organisms that glow in the dark, like fireflies, but with a blue light that travels well in water. About 40 years ago, scientists noted that these bacteria make light only when their populations reach a critical cell number. Some sort of chemical inducer that accumulated with increasing cell density had to be involved. “Bioluminescence is fantastic for my group,” Bassler said, explaining that the light, while very pretty, isn’t important in and of itself. What’s important about bioluminescence is that it makes a wonderful marker for quorum sensing. “We can just turn the lights off in the room and see it.” Callout: “Bioluminescence is fantastic…it makes a wonderful marker for quorum sensing, for chemical communication.” Vibrio fischeri, the first luminescent quorum sensing bacterium studied, lives as a symbiont. One of its hosts, the Hawaiian bobtail squid, has two lobes under its mantle that function as a light organs. Lots of Vibrios live in these light organs; they’re in there making autoinducers. The V. fischeri glow and in exchange the quid feeds them. The light organ is loaded with amino acids and sugars, it’s like a candy store for bacteria. “If you’re a V. fischeri, it’s a much richer, happier, fatter life being in this squid than fending for yourself in the open ocean,” said Bassler. From the bacterium’s point of view, bioluminescence means free food. And of course the squid wants to keep these bacteria happy. It uses their light as an anti-predation device. Callout: The V. fischeri glow and in exchange the squid feeds them. The little bobtail squid lives just off the coast of Hawaii in shallow, knee deep water. It’s nocturnal. During the day the squid buries itself in the sand and sleeps, coming out at night to hunt. On very bright nights when there’s a lot of starlight or moonlight, the light penetrates the pools of water. The squid has detectors on its back that tells it how much light is hitting the water. Using its ink sack as a shutter, the squid lets out exactly the same amount of V. fischeri-generated light below as that coming from above so the squid doesn’t make a shadow. In other words, the squid counter illuminates itself against predators that could find and kill it if they saw its shadow. [Insert Slide #2: New title: Squid’s Night Out With V. fischeri] When the sun comes up the squid and buries itself back in the sand to sleep and pumps out 95% of the bacteria. The number of V. fischeri plummets, the signal molecules disappear and the light goes out. During the day the remaining bacteria replicate, release autoinducers, and by night the light comes on exactly when the squid needs it. The whole system, a squid “chemostat,” is controlled by circadian rhythm. In the mid-1980s, bacterial luminescence caught the attention of Mike Silverman and Joanne Engebrecht at the Agouron Institute in La Jolla, California. Fascinated, they took the V. fischeri chromosome, chopped it up into big pieces and put “the whole mess” into recombinant Escherichia coli. Then they looked for E. coli that could glow in the dark. Not only did the E. coli glow, they lit up only at high cell numbers and made the V. fischeri signal molecule. Thus, said Bassler, “Engebrecht and Silverman got the luciferase enzymes and also the density-sensing mechanism from one piece of DNA.” They named the gene that made the light-producing enzyme “lux,” after the Latin for “god of light.” Callout: Not only could the E. coli with V. fischeri genes glow, they lit up only at high cell numbers. The luxI (“I” for “inducer”) gene encodes a protein that makes an AHL signal molecule (AI-1) which freely diffuses in and out of the bacterial cell, collecting in the microbial environment. When the LuxI signal molecules reach a critical level, partner proteins called LuxR (“R” for “regulation”) bind enough of them to turn on the genes encoding the enzymes that make light. “It’s a very simple circuit,” according to Bassler. [Slide #3. Quorum Sensing] “The more cells there are, the more signal molecules are generated and eventually the light goes on.” Hundreds of LuxIR-type quorum-sensing circuits have been found in Gram-negative bacteria during the past decade. They invariably make signal molecules that bind to partner proteins and the resulting complexes turn on genes that bacteria express when they’re in a community. Notably, the genes regulated by quorum-sensing controlled behaviors don’t do isolated bacteria any good. And there is good reason for this, said Bassler. For example, if a few bacteria get into an enormous eukaryotic host the worst thing for them to do is to start randomly secreting their toxins. “It’s more productive for tiny little cells to count themselves with quorum-sensing molecules, and when there are enough of them, launch an attack together. That’s the only way they can successfully outwit a huge organism.” Callout: The only way tiny little cells can outwit a huge eukaryotic organism is to count themselves with quorum-sensing molecules and when there are enough of them, launch an attack together. Better living through chemistryAlthough they share a propensity for making light, V. fischeri and its free-living relative V. harveyi have different circuitry controlling bioluminescence. By making thousands of V. harveyi mutants, Bassler and her colleagues discovered that V. harveyi needs two autoinducers for quorum-sensing gene expression. Its AI-1, an AHL derivative, is highly specific and is detected by V. harveyi’s cytoplasmic membrane sensor protein LuxN. Another autoinducer, AI-2, depends on two proteins for detection, LuxP and LuxQ. LuxP is a periplasmic binding protein and LuxQ is a two-component hybrid sensor kinase embedded in the bacterial inner membrane. [Slide #5. Quorum Sensing in V. harveyi] Callout: V. harveyi responds to two autoinducers: AI-1, a private language, and AI-2, which turned out to be an interspecies communication molecule. LuxN, LuxQ and other two-component proteins provide bacteria with a way to “see” their world. A sensory domain in the bacterial membrane protrudes outside to detect environmental stimuli. Information from both LuxQ and LuxN feed into a two-component protein called LuxU that sends the signal to a final protein called LuxO, which, in turn, controls luciferase and bioluminescence. All bacterial two-component systems are controlled by a phosphorylation cascade involving a sensor histidine kinase and an aspartate receptor response regulator. Eureka!Why, Bassler wondered, if they end up in same the place, does V. harveyi need two signals to make light? After collecting every bacterium they could find and exposing V. harveyi to cell free culture fluids from these different species, they saw that nearly all the other bacterial species produced the second molecule AI-2. The group had found new bacterial language, a universal one: AI-2. This was a gigantic discovery. “Everywhere V. harveyi lives in the wild, it mixes with hundreds of other species of bacteria,” Bassler told the audience. “It needs to know more about what’s going on in the world than it can find out from its own species alone. V. harveyi has to take a census of the other players in its community.” In contrast, V. fischeri spends most of its time among relatives in a secure host, so what other species are doing probably doesn’t make all that much difference to them. Wanting to know more about V. harveyi’s conversations with other species, Bassler designed a mutant strain that could light up only in the presence of another microbe’s AI-2. When she put the reporter strain on a petri plate with E. coli and Salmonella, the lights went on. The mutant V. harveyi were responding to AI-2 diffusing across the plate from the E. coli and Salmonella. [Slide #6. Quorum Sensing in E. coli and Salmonella ] But the mutant V. harveyi didn’t recognize every E. coli; they ignored a very domesticated strain, DH5α, that’s been used in laboratories for almost 100 years. The wilder and more virulent bacteria are, the more AI-2 they seem to generate, and DH5α made none. Callout: The wilder and more virulent bacteria are, at least in the laboratory, the more AI-2 they seem to generate. This docile strain of E. coli showed Melissa Miller, a graduate student in Bassler’s group, the way to find the gene responsible for AI-2 production. Miller took an entire wild-type library of V. harveyi genes and put them one by one into DH5α until she found the gene that gave DH5α back its universal voice and called it luxS. Additional research showed that luxS is broadly conserved and widely spread in the bacterial community. [Slide #7. Bacteria that Contain LuxS] Every bacterial species reported to contain the luxS gene and consequent enzyme was tested in Bassler’s laboratory and all made AI-2. However, Bassler cautioned that the bacteria investigated may seem like a Who’s Who of pathogens, but the list is incredibly skewed because people tend to sequence only medically important microbes. She emphasized that V. harveyi also speak AI-2 and “they wouldn’t even hurt a fish,” indicating just how broadly spread the luxS gene must be. Furthermore, luxS is ancient. Obviously, said Bassler, interspecies communication arose before Gram-negative and Gram-positive bacteria split into two separate groups and that was a very long time ago. Callout: However, V. harveyi also speaks AI-2 and “they wouldn’t even hurt a fish,” so the LuxS gene must be very broadly spread among bacteria. The elusive god of lightAlthough luxS was ubiquitous in bacterial genomes, Bassler and her colleagues found that determining LuxS’s function was elusive and AI-2 couldn’t be purified using traditional methods. Then Stephan Schauder, a postdoctoral fellow in Bassler’s laboratory, discovered that Borrelia burgdorferi, the causative agent of Lyme disease, has luxS in an operon with two other genes with known functions, metK and pfs. [Slide #8. Genomic sequence of Lyme disease spirochete, Borrelia burgdorferi] These genes work in the S-adenosyl methionine (SAM) pathway and the luxS-encoded enzyme, LuxS, turned out to be the third enzyme in a three-step conversion of SAM to DPD and ultimately to AI-2.[Slide #9. SAM Utilization] Callout: Although luxS is widely spread over bacterial genomes, its function proved elusive –mapping all over the place– and AI-2 was difficult to purify by traditional methods. The next step, identifying the chemical structure of AI-2, proved even more difficult. Bassler with her colleague Fred Hughson determined the crystal structure and molecular weight of AI-2 from V. harveyi. They proposed a carbon-oxygen configuration. But a neighboring chemist told them: “That molecule may exist at the core of the sun for a few nanoseconds, but it doesn’t exist on earth. A carbon cannot have four oxygens on it for very long, it’s too unstable.” However, boron sits right next to carbon on the periodic table of elements, it’s only one mass unit different and the two can’t be distinguished with spectrometry. But unlike carbon, boron can bond with four oxygens. Eventually the structure of AI-2 and the hydrogen bond network that stabilizes it in the LuxP binding site was revealed. It contains two fused five-membered rings held within the LuxP binding site by polar interactions. [Slide # 14. New title: AI-2 in the LuxP Binding Site] However, both E. coli and Salmonella typhimurium can tell V. harveyi when to light up which proves that AI-2 signaling isn’t limited to vibrios. While looking around Salmonella chromosomes for AI-2 controlled genes, two members of Bassler’s laboratory, Michiko Taga and Karina Xavier, found an operon without an assigned function and named it “Lsr" for “luxS-regulated” operon. [Slide #16: The Salmonella Lsr Operon] LsrB, like the AI-2 signal receptor in V. harveyi, transports AI-2. Moreover, both the LuxP and LsrB ligands are derived from the same precursor, DPD. [Slide #21. A Chemical System of Interconverting Molecules] there’s isn’t a boron ring on the Salmonella molecule, said Bassler, which makes sense because the ocean is loaded with boron and it’s easy for V. harveyi to find, but terrestrial environments, where Salmonella lives, are boron-poor and carbon-rich. Callout: AI-2 is a mixture of interconvertible molecules, more than one of which is important for interspecies signaling. These studies showed that AI-2 is a mixture of interconvertible molecules and more than one is important for interspecies signaling. That’s to be expected because different organisms use LuxS-based signaling for very different reasons, said Bassler. It’s naďve to expect that these are the only two molecules conveying information in bacteria but “we think they’re all going to be based on these two reactions because those are the two closed forms that can happen with reasonable chemistry.” All or nothingCallout: Bacteria are making all or nothing decisions all of the time, one misstep and it’s all over. When a bacterium decides between acting as an individual or going along with the group, it’s an all-or-none-decision. Information about the population has to be integrated and transduced into the cells with high fidelity because wrong actions would be disastrous. Thus, the next pathway Bassler explored was the one that enables bacteria to convert extracellular population-density information into intracellular signals that change gene expression, cellular physiology, and group behavior. Genetic analyses pointed to the importance of a regulatory component known as LuxO, which belongs to a family of two-component proteins known to interact with the alternative sigma factor s54 to turn on genes. The bacteria they chose to investigate were V. harveyi and its rather noxious relative, Vibrio cholerae. [Slide #26. Quorum Sensing in V. harveyi and V. cholerae] Callout: LuxO had every bell and whistle that would make it an activator, but it wasn’t. “All known two-component proteins similar to LuxO were activators,” said Bassler, “and LuxO had every bell and whistle that would make it an activator. The problem was when we knocked it out, quorum sensing stayed on.” Something else had to be involved, some sort of repressor that shuts off the transcription factor historically named “LuxR” (not to be confused with the regulator LuxR from V. fischeri). One suspect bacterial protein was Hfq, which has been known for about 40 years. “And in that time it’s been given all these magical properties; it’s supposed to do everything, but in fact it does only one thing,” said Bassler. “Hfq is just a chaperone protein for small RNAs, regulatory RNAs.” Further research showed that at low cell density, in the absence of autoinducers, LuxO turns on multiple small Hfq-bound sRNAs, and they silence LuxR/LuxCDABE in V. harveyi and its equivalent in V. cholerae called HapR. A scan of vibrio chromosomes showed that V. cholerae had four quorum regulatory RNAs (QRRs). [Slide #30. Alignment of all QRR sRNAs] Callout: sRNAs and their chaperone proteins, Hfqs control the critical transition of a bacterium from a solitary to a social cell. When the sRNAs were deleted one at a time, nothing happened. Quorum sensing was suppressed only when all four were deleted at once. [Slide #32. Simultaneous Deletion of Qrr-4 is Required to Affect Quorum Sensing] These findings led Bassler to conclude that Hfqs together with sRNAs create an ultrasensitive regulatory switch that controls the critical transition of a bacterium into its quorum-sensing mode. An obvious question, said Bassler, is why four sRNAs have to be knocked out together for the light to go on. She speculated that it probably has to do with V. cholera’s lifestyle. “Sometimes they’re in the gut, sometimes in biofilms, sometimes in seawater. It’s possible there are different regulatory sites upstream of each sRNAs; we’re exploring that right now.” How it worksThe quorum-sensing circuit that controls bioluminance in V. harveyi and virulence in V. cholerae can be summarized as follows [Slide #31. Quorum Sensing in V. harveyi and V. cholerae]: Lights off. All bacterial two-component systems function by a conserved phosphorylation cascade involving a sensor kinase and response regulator pairs. In the case of quorum sensing, when bacterial populations are sparse and autoinducers absent, the sensor kinases in the LuxNQ regulator domains autophosphorylate at the histidine residues and the phosphate is transferred to partner aspartate residues. The phosphate is sequentially transferred via LuxU to LuxO. Phospho-LuxO and σ54 induce sRNAs that, together with Hfq, prevent LuxR from functioning. This keeps quorum sensing (and the light) turned off. Lights on: At high cell density, AI-1 (an AHL), and AI-2 (the product of LuxS) are detected and bound by LuxN and LuxPQ, respectively. This leads to the dephosphorylation of LuxU and LuxO. The sRNAs are not made, so LuxR is free to turn on quorum sensing genes such as those encoding luciferase (LuxCDABE). Deceit & deceptionPeople shouldn’t think that all bacteria are kindly and cooperative, Bassler said, there’s a lot of “shenanigans” going on out there. In fact, an entire microbial mafia is emerging. For example, there are bacteria armed with lactonases that cleave the AHL signals of competing cells so they can’t be heard. Some “stealth” bacteria—notably E. coli and Salmonella typhimurium—interfere with the ability of other species to assess and correctly respond to cell-density changes by manipulating their own AI-2 and making themselves invisible. Pseudomonas aeruginosa infecting the lungs of patients with cystic fibrosis doesn’t make AI-2s itself, but listen in on the signals made by neighboring bacteria and turns on its virulence program when it detects sufficient cells in the vicinity. Furthermore, there is evidence that manipulation of quorum sensing-controlled processes may also occur in bacterial-eukaryotic associations. Of course, there’s a lot of chemical warfare going on. That’s where we humans stole most of our antibiotics from. And on that note, this exceptionally informative and fascinating session drew to a close. Open QuestionsSome bacteria flourish in the presence of viral infection. Could they be cross-talking with viruses or are they reacting to the host’s inflammatory response? Small RNAs haven’t been as extensively studied in prokaryotic cells as they have in eukaryotic ones. Now that this is changing, is anyone exploring the interactions between the two domains of life? Fireflies use luciferase bioluminescence to communicate with each other. Quorum sensing molecules turn the lights on in vibrios but what does the light do for them once it’s on? ResourcesWeb Sites American Society for Microbiology Center for Biofilm Engineering www.molbio.princeton.edu/research Journal Articles Bassler, B.L., Losick,R. 2006. Bacterially Speaking. Cell, 125:237-246
Bassler, B. L. 2002. Small talk: cell-to-cell communication in bacteria. Cell 109: 421-424.
Bassler, B. L., M. Wright, R. E. Showalter & M. R. Silverman. 1993. Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol. Microbiol. 9: 773-786.
Bassler, B. L., M. Wright & M. R. Silverman. 1994. Sequence and function of LuxO, a negative regulator of luminescence in Vibrio harveyi. Mol. Microbiol. 12: 403-412.
Camilli, A. & B. L. Bassler. 2006. Bacterial small-molecule signaling pathways. Science 311: 1113-1116. Chen, X., S. Schauder, N. Potier, et al. 2002. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549.
Engebrecht, J. & M. Silverman. 1984. Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA 81: 4154-4158. Engebrecht, J. & M. Silverman. 1987. Nucleotide sequence of the regulatory locus controlling expression of bacterial genes for bioluminescence. Nucleic Acids Res. 15: 10455-10467. FULL TEXT Federle, M. J. & B. L. Bassler. 2003. Interspecies communication in bacteria. J. Clin. Invest. 112: 1291-1299. FULL TEXT
Henke, J. M. & B. L. Bassler. 2004. Bacterial social engagements. Trends Cell Biol. 14: 648-656.
Lenz, D. H., K. C. Mok, B. N. Lilley, et al. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
Miller, S. T., K. B. Xavier, S. R. Campangna, et al. 2004. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol. Cell 15: 677-687. Showalter, R. E., M. O. Martin & M. R. Silverman. 1990. Cloning and nucleotide sequence of luxR, a regulatory gene controlling bioluminescence in Vibrio harveyi. J. Bacteriol. 172: 2946-2954. FULL TEXT Taga, M. E. & B. L. Bassler. 2003. Chemical communication among bacteria. Proc. Natl. Acad. Sci. USA 100(suppl.2): 14549-14554. FULL TEXT
Waters, C. M. & B. L. Bassler. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21: 319-346
Xavier, K. B. & B. L. Bassler. 2005. Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J. Bacteriol. 187: 238-248.
Xavier, K.B. & B. L. Bassler. 2005. Interference with AI-2-mediated bacterial cell-cell communication. Nature 437: 750-753. From the AcademyeBriefings Wiping the slate clean: enzymatic detachment of bacterial biofilm, featuring Jeffrey B. Kaplan. 2004. New York Academy of Sciences eBriefing, sponsored by the Emerging Infectious Diseases Discussion Group. Knowing your neighbors: early quorum sensing and infection, featuring Jesse S. Wright. 2004. New York Academy of Sciences eBriefing, sponsored by the Emerging Infectious Diseases Discussion Group. Speaker
Bonnie L. Bassler, PhD Bassler, who was elected to the National Academy of Sciences in 2006, is a Howard Hughes Medical Investigator and Professor of Molecular Biology at Princeton University. She received a B.S. in Biochemistry from the University of California at Davis and a PhD in Biochemistry from Johns Hopkins University. Bassler performed her postdoctoral work in genetics at the Agouron Institute, and joined the Princeton faculty in 1994 where she is the Director of Graduate Studies in the Department of Molecular Biology. The research in her laboratory focuses on the molecular mechanisms bacteria use for intercellular communication in a process called quorum sensing. Bassler was awarded a MacArthur Foundation Fellowship in 2002. She was elected to the American Academy of Microbiology in 2002 and made a fellow of AAAS in 2004. In 2003 Bassler received the Theobald Smith Society Waksman Award and is the recipient of this year’s ASM Eli Lilly Investigator Award. 2006 Eli Lilly and Company Research Award Laureate Bassler is an editor for Molecular Microbiology and Annual Reviews of Genetics, and an associate editor for the Journal of Bacteriology. She serves on grant, fellowship, and award review panels for the NSF, ASM, AAM, Keck Foundation, and the Burroughs Wellcome Trust. Marcia Stone, a science writer based in New York City and longtime member of the Academy’s microbiology section, discovered bacterial genetics at the Harvard Medical School in the late1980s and has been an avid fan of prokaryotes ever since. More of her work can be found at http://www.mstoneworks.net |
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