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Shedding Light on the Bioluminescence “Paradox” Although Luminescence Provides Host Squids with Obvious Advantages, How Does It Benefit Light-Producing Bacteria?

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Shedding Light on the Bioluminescence “Paradox” Although Luminescence Provides Host Squids with Obvious Advantages, How Does It Benefit Light-Producing Bacteria? Shedding Light on the Bioluminescence “Paradox” Although luminescence provides host squids with obvious advantages, how does it benefit light-producing bacteria? Eric V. Stabb he fascinating biochemistry, genetics, have special significance for this bacterium. Bi- and cell density-dependent regula- oluminescence offers many such puzzles, and it tion of bacterial bioluminescence is unlikely a single solution will solve them all. T provoke a challenging question. Nonetheless, it is an exciting moment in bio- What good is it to bioluminescent luminescence research, with recent advances of- bacteria? fering the promise of answering the longstand- There may be no single answer to this seem- ing question, “how can bioluminescence ingly simple question. However, two recent ad- help bacteria?” Although researchers learned vances shed new light on the problem. First, nearly a century ago that luminescence reduces studies of the symbiosis between the biolumines- oxygen and that symbiotic bacteria inhabit the cent bacterium Vibrio fischeri and the Hawaiian light organs of squids, what was unimaginable bobtail squid bring an ecologically relevant until very recently is our ability to analyze the V. niche for a bioluminescent bacterium into focus fischeri genome sequence and to combine this under the discerning lens of controlled labora- knowledge with the ability to genetically manip- tory experimentation. Second, progress in under- ulate these bacteria and observe them under standing the genetics of V. fischeri, including controlled laboratory conditions in the ecologi- genomic sequencing of a squid symbiont, is en- cally relevant environment of a natural squid abling researchers to analyze how luminescence host. integrates into the physiology of this bacterial species and to test specific hypotheses about Biochemistry and Genetics of what advantage light production confers on the V. fischeri Bioluminescence bacteria. In bacteria such as V. fischeri, light is generated Understanding how bioluminescence aids V. by an enzyme, luciferase, that contains two pro- fischeri in a squid light organ will likely not be teins, designated LuxA and LuxB (Fig. 1). the final word on how bioluminescence benefits LuxAB sequentially binds FMNH2,O2, and an bacteria. Differences among bioluminescent aliphatic aldehyde (RCHO) that are converted bacteria intimate that this ancient system con- to an aliphatic acid, FMN, and water. In turn, fers varied selective advantages. For example, they are released from the enzyme with the con- “cryptically luminescent” Vibrio pathogens, comitant production of light (Fig. 1A). Addi- such as Vibrio salmonicida, produce luciferase, tional proteins, LuxC, LuxD, and LuxE, are the enzyme responsible for bioluminescence, but responsible for (re)generating the aldehyde, little or no aldehyde substrate, and may use while another protein, LuxG, shuttles reducing Eric V. Stabb is an luciferase to form “dark reaction” hydrogen power from NAD(P)H to FMN to (re)generate Assistant Professor peroxide as a host-damaging virulence factor. FMNH2. in the Department In contrast, some strains of Vibrio logei pro- In V. fischeri, the luxC, luxD, luxE, and luxG of Microbiology at duce an accessory Y1 protein that shifts their genes flank luxA and luxB. These genes are the University of emitted light to a yellow wavelength, which may cotranscribed with luxI, while luxR is adjacent Georgia, Athens. Volume 71, Number 5, 2005 / ASM News Y 223 FIGURE 1 ulated when intracellular AI concentra- tion exceeds a threshold. Thus, light is produced at high cell densities, such as A Biochemistry and physiology during growth in a squid light organ, Substratered Substrateox but not when planktonic cells are grow- ing at low densities. O e– transport 2 NADH NAD+ H+ LuxG Bioluminescence at First Analysis + H motive force H2O Appears To Be a Drag on Cell Energy FMNH2 FMN Despite having a good understanding of ATP Products LuxAB the biochemical and genetic mechan- FMN ics of bioluminescence, researchers re- main uncertain over what its selective LuxAB LuxAB -FMNH2 advantage is to bacteria. In particular, H O O 2 the apparent costs in energy to cells 2 from bioluminescence make its exis- tence appear paradoxical. Light In addition to the sizable biosyn- O - 2 LuxAB -FMNH2 thetic cost in producing the Lux pro- LuxE + LuxC RCHO RCOOH teins, generating light consumes both biochemical reducing power and oxy- + NADP NADPH + ATP gen, seemingly competing for substrates LuxD + AMP + PPi with aerobic respiration, which recovers O2- LuxAB -FMNH2 energy through electron transport (Fig. acyl-ACP 1A). Furthermore, energy stored as ATP RCHO is consumed in regenerating the alde- hyde substrate (Fig. 1A). B Genetics and quorum sensing Indications that bioluminescence luxR luxI luxC luxD luxA luxB luxE luxG hinders cultured cells date at least as far back as E. Newton Harvey’s work at Princeton University in the early 1900s. Generate light Those findings were extended by J. Woodland (Woody) Hasting at Harvard OO University and his collaborators, who O showed that some relatively darker mu- N tants outgrew their brighter parents. Sim- H LuxR O LuxI ilarly, Paul Dunlap, now at the University AI-dependent Autoinducer (AI) of Michigan, characterized bright mu- transcriptional activator tants of V. fischeri that grew more slowly than do their relatively dim parent. V. fischeri bioluminescence. (A) Biochemistry and physiology. (B) Genetics and quorum In 1980, Ken Nealson and David Karl, sensing. currently at the University of Southern California and the University of Ha- waii, respectively, also found that cells to the other lux genes but not transcribed with expend appreciable energy for luminescence. them (Fig. 1B). Together LuxI and LuxR under- However, these two researchers did not find that lie a well-characterized quorum-sensing regula- bioluminescence slows growth rates. tory circuit, in which LuxI generates an autoin- These apparently inconsistent findings are dif- ducer (AI) that interacts with LuxR to stimulate ficult to interpret. Part of the explanation for lux transcription. The expression of lux is stim- the inconsistencies is that the best technology 224 Y ASM News / Volume 71, Number 5, 2005 Stabb’s Science: from Insects and Owls to Bioluminescent Bacteria and Squids Eric Stabb’s parents, both chemis- cards telling applicants when to E. scolopes hatchlings lack symbi- try teachers, encouraged his scien- be on hand for a phone interview,” onts but soon obtain V. fischeri tific interests from a very early age. he says. But the postcard arrived from their surroundings. Once When he became fascinated with too late for him to hold such an inoculated, an individual squid insects at age 8, his father made interview, scuttling his chances to carries V. fischeri cells in epitheli- him a butterfly net and mounting spend a summer doing field stud- um-lined crypts of a specialized board, and supplied him with glass ies in Alaska. organ. Light produced by those slides, pins, and, soon, his own In this case, zoology’s loss was bacterial cells helps the squid elude “knockout” jar plus a supply of car- microbiology’s gain. Stabb had predators, while the host squid bon tetrachloride. “They wouldn’t submitted what he calls a “fall- provides V. fischeri with nutri- let us use that stuff in college, and back” application to a program ents. I had a bottle at age 10,” Stabb sponsored by the National Sci- “I think it’s cool,” Stabb says, says. Soon those early insect-ori- ence Foundation to support un- referring to that symbiosis. “ I’m ented interests shifted, and he de- dergraduate research. He was ac- fascinated by bioluminescence and veloped a special liking for owls. cepted into this program, run by by the biology of the symbiosis.” He was so analytically minded as ASM-Carski Distinguished Teach- It also has a “gee whiz” appeal for a youngster that he collected owl ing Award recipient Ken Todar, students, he adds. “This is some- pellets, “looking for jawbones to and worked with Tim Donohue thing students can get fired up see what they had eaten,” he ad- studying photosynthetic bacteria. about, and it’s something they can mits. “I’m sure I sometimes left “I had no idea what microbiology learn experimental biology with. I them out, but I don’t remember was all about,” Stabb recalls. “I don’t know if my research will my mom ever complaining.” got hooked by what you could do have other practical benefits down Instead, his parents happily sup- experimentally with bacteria, es- the road—maybe, maybe not. But plied him with scientific kits, ma- pecially genetically.” Once hooked, I surely hope that some good sci- terials, and other support without he signed up to do more research, entists will get a start here.” being asked, he recalls. It was as if another course, and became “thor- Stabb, who grew up in Janes- “all my early grants were funded, oughly sold on prokaryotes.” ville, Wis., near the Rock River, is except most of the time I didn’t Stabb and his older brother, an avid runner. He competed in even apply for them,” he says. “It who holds a doctorate in applied high school and college, and still was like having a program man- physics and co-owns an engineer- trains for regular track sessions ager who anticipated what you ing consulting company, both with a group of running buddies. might want—and got it for you.” earned nearly straight A’s in their He and his wife Janice Flory, who Stabb, 37, now follows the con- high-school science courses, but ventional grant application pro- each with one exception. “He got is a project coordinator for the cess along with his teaching duties a B in physics, and I got one in Georgia Coastal Research Coun- in his professional role of assis- biology,” Stabb says. “There is cil, live in a neighborhood near tant professor in the department probably some deeper significance the UGA campus.
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