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This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute.

Notice: © 2001 McGraw-Hill. This manuscript is an author version with the final publication available and may be cited as: Widder, E. A. (2001). Bioluminescence. In McGraw-Hill yearbook of science & technology 2001 (pp. 52-55). New York: McGraw-Hill.

McGRAW-HILL YEAitBOOK OF ctence• Techiiology

2001

Comprehensive coverage of recent events and research as compiled by the staff of the McGraw-Hill Encyclopedia of Science & Technology

McGraw-Hill New York San Francisco Washington, D.C. Auckland Bogota Caracas Lisbon London Madrid Mexico City Milan Montreal New Delhi San Juan Singapore Sydney Tokyo Toronto 52 Bioluminescence

top view based studies, and microscopy, scientists are poised to greatly increase the understanding of how microbes live attached to a surface. For backgronnd information see ANITBIOTIC RESIS­ TANCE; BACTERIAL GENETICS; BIOfllM; FUNGI; MEOI­ CAL BACTERIOLOGY in the McGraw-Hill Eng-dope­ dia of Science & Technology. George O'Toole Bibliography. ]. W. Costerton et al., Microbial bio­ films,Annu. Rev.Microbiol,49:711-745, 1995; D. G. Davies et al., The involvement of cell-to-cell signals in the development of a bacterial biofilm, Sdence, 280(5361):295-298, 1998; M. Givskovetal., Eukary­ otic interference with homoserine lactone-mediated prokaryotic signalling, J Bacterial., 178(22):6618- side view 6622, 1996; A. T Henrici, Studies of freshwater bac­ teria, L A direct microscopic technique, j Bacte­ rial., pp. 277-287, 1933; P. E. Kolenbrander and]. London, Adhere today, here tomorrow: Oral bacterial (a) adherence.] Bacterial., 175(11):3247-3252, 1993; ]. R Lawrence et al., Optical sectioning of microbial biofilms, j Bacterial., 173(20):6558-6567, 1991; wild type mutant G. A. O'Toole et aL, Genetic approaches to the study of biofilms, Metb. Enzymol., 310:91- 109, 1999; G. A. O'Toole, H. Kaplan, and R Kolter, Biotilm formation as microbial development, Annu. Rev. Microbial., 54:49-79, 2000; G. A. O'Toole and R Kolter, Flagellar and twitching motility are neces­ sary for Pseudomonas aeruginosa biotilm develop­ ment, Mol. Microbial., 30(2):295-304, 1998; L S. Thomashow and D. M. Weller, Current concepts in (b) the use of introduced bacteria for biological disease control: Mechanisms and antifungal metabolites., in Fig. 3. Testing for biofilm formation. (a) 96-well dish. G. Stacey and N. Keen (eds.), Plant Microbe Interac­ (b) Wild type leaves a dark ring; mutant bacteria do not form a ring. tions, Chapman and Hall, New York, 1995.

researchers that they are looking at an aspect of the bacterial lifestyle that is poorly understood or bas Bioluminescence not been studied in any detail at the level of the Bioluminescence, which is the ability of an organ­ gene. ism to emit ~ible light, is a common attribute of Future research. While understanding the biology marine creatures. The phenomenon is relatively rare of biofilm formation is an important endeavor, long­ on land, where fireflies are the best-known exam­ term goals also include devising new strategies for ple. In the oceans it is ubiquitous, and is found at controlling biofilm formation. Implant-based infec­ all depths. The most common sources in the ma­ tions are an increasing problem in clinical settings. rine environment are bacteria, dinoflagellates, jelly­ Recent studies also implicate biofilm formation in fish, crustaceans, cephalopods, and fish. Among infectious diseases, including the infections associ­ cephalopods, which indude squids, cuttlefish, and ated with cystic fibrosis. Biofilms can also lead to the octopods, the expression of bioluminescence is clogging of pipelines and contamination in industrial extremely diverse. Out of 100 genera of squids and processes. Another current area ofstudy is the search cuttlefish, 63 have been fonnd to include biolumi­ for new means to control the formation of biofilms. nescent spedes, but in octopods only 3 out of One class of recently discovered compounds that can 43 genera do. interfere with the formation of biofilms is the fura­ Evolution. Bioluminescence is produced when an nones. Furanones,i which are analogs of homoser­ enzyme, known as luciferase, catalyzes the oxidation ine lactones, were briginally isolated from a particu­ of a substrate, known as luciferin, by molecular oxy­ lar marine alga that was unusually free of microbial gen. Luciferase and luciferin are generic designations biotilms (most algae are covered with bacteria). The for any enzyme or substrate involved in a biolumi­ furanones appear to interfere with the development nescent reaction. Based on the number of different of the typical biofilm structure and apparently render chemistries and the variety ofexpress ions of biolumi­ these organisms more susceptible to treatment with nescence in different organisms, it appears that the natural biocides. Using bacterial genetics in conjnnc­ ability to produce light arose independently many tion with the newest molecular techniques, genome- different times in many different groups of animals. Bioluminescence 53

Titis remarkable degree of convergent evolution is a dear indication of the selective advantages afforded by light production. The prevalence of bioluminescence in the open ocean is believed to be a consequence of selection pressures imposed by the struggle to survive in an environment that lacks hiding places. There are no uees or bushes to hide behind in the vast expanses of the open ocean, constituting most of the living space on Earth. However, survival frequently depends on the ability to hide from predators. During evolution­ ary history, as the oceans filled up with ever swifter and more ferocious predators, many prey that could not outswim them found refuge in the dark depths. Among these were many that depended on vision and visual signals to attract mates, to lure prey, and to avoid predators. As these vision-dependent animals colonized the twilight depths of the ocean, natural selection favored those with enhanced \-isual sensi­ tivity and amplified visual signals. Bioluminescence is one way to enhance a visual signal in an environment with little light. For exam­ ple, the ink used by a squid or an octopus to distract or confuse a predator has little or no visual impact Fig. 1. Location of bioluminescence (indicated in color) in ~ dark depths. However, releasing bioluminescent the octopus Japetella diaphana. (Redrawn from P. J. ·chemicals directly into the water serves as a highly Herring, Luminescent organs, in E. R. Trueman and M. R. ef(ective distraction, and is a common trick of many Clarke, eds., The Mollusca, vol. II, Academic Press, New Yorlc) deep-ocean dwellers, including some shrimp, jelly­ fish, squid, and fish. Similarly, visual signals such as lures used to attract prey or body parts displayed Differences in light organ distribution between to attract a mate, are made visible by biolumines­ males and females, which are usually taken as ev­ cence. Many animals also have bioluntioescem head­ idence that they function in sexual signaling, are lamps that they can use to help them see in the rare in squid and cuttlefish. However, in two of dark. Bioluminescence can also function as camou­ the tltree genera of octopods with luminescent spe­ flage. In the depths between 200 and 1000 m (660 cies, the bolitaenids Japetella and EledoneUa, light and 3300 ft), sunlight filtering down tltrough sur­ organs take the unusual form of a ring around the face waters creates a dim background light when mouths of breeding females (Fig. 1). The fact that viewed from below. Against this background, the sil­ these light organs occur only in breeding females houette of an opaque animal is an easy target for and actually disappear following spawning pro­ an upward-looking visual predat01: Many fish, squid, vides sound evidence that they function in sexual and shrimp camouflage their silhouettes by pro­ signaling. ducing downward-directed bioluminescence that The only other confirmed case of bioluminescence exactly matches the color, intensity, and angular dis­ among octopods is in the deep-sea cirrate (finned) tribution of the background light field. octopus Stauroteuthis syrumsis (Fig. 2). Although Ught organs. light organs in cephalopods run the this octopus was first described in 1879, it was not gamut from simple patches of light-producing tissue until 1999, when a live specimen was collected to elaborate light organs known as pbotophores that using a midwater submersible, that it was discovered contain complex optical elements such as lenses, fil­ to be bioluminescent. When this specimen, which ters, irises, reflectors, and shutters. Although there was collecte d from 755 m (2490 ft) in the Gulf of is little direct evidence for the functions served by l'rlaine, was placed in a shipboard aquarium, re­ these light organs, their anatomical locations often searchers were surprised to note that its "suckers• provide some hint as to their purpose. For example, did not stick to anything, and moreover that these in many otherwise transparent squid, phptophores suckers were capable of emitting blue light may occur beneath pigmented structures s1Jch as the (Fig. 3). l eyes or liver, and it is thought that luminescence An investigation of the anatomy and ultrastructure serves to eliminate the shadows that these opaque or­ of the suckers-photophores revealed that although gans would cast. Similarly, many opaque squid have these organs still had sucke.rlike traits, light­ photophores arrayed over most of the underside of producing cells replaced many of the muscles that their bodies, and these too can provide camouflage. are prominent features of normal suckers. In effect, Ught organs are also found on arms and tentacles, they appear to be light organs that have evolved perhaps serving as sexual signals or lures to attract from suckers. Because there is no fossil record prey. of bioluminescence, the evolutionary history of 54 Bioluminescence

be assumed that under such circumstances biolu­ minescence function defen ively, sen·ing either to startle a p redator or to auract larger secondary pre­ dators that may prey on the primary predaror. An additional funCtion for bioluminescence in these octopods may be as an attractant fo r their primary yrey items, which are copepods. These tiny crus­ taceans, which are like the insects of the sea, seem an odd food choice for such a large, slow-moving animal. However, if the light organs act as a lure, attracting the copepods like moths to a flame, then perhaps this strange diet makes sense. When seen from submersibles, the posture of this octopus, w ith arms spread out in an umbrella or beU-shaped atti­ tude, seems consistent with the idea that it uses its light organs as lures. Additionally, the blue light emit· ted by the suckers-photophores is a good match for the color that travels farthest through seawater, and therefore should be highly visible to potential prey. Once the copepods are attracted to the light, they may become enmeshed in a mucous web, which the octopus secretes from glands near the mouth. Since there are only the three confirmed cases o f bioluminescence in octopods ( in the cirrate

Fig. 2. Deep-sea finned octopus Stauroteuthis syrtensis. (Photo by E. Widder/Harbor Branch Oceanog. © 1999)

light-producing structures is difficult to deduce. Therefore, such light organs, which retain some in· dication of their previous function, offer Yaluable insight into that evolutionary history. In this case it is postulated that the change from sucker to light organ may have occurred during colonization of the deep open ocean by a creature that was ori· ginally a shallow-water bottom dweller. Once the suckers were no longer useful for clinging to the bot­ tom, their only remaining value may have been for communication. ShaUow-water species of octopus display their suckers for (nonbioluminescent) sexual signaling. In the dim depths such displays would lose visual impact unless amplified. One way to enhance visibility would be to evolve highly reflective suckers, which is in faCt a n otable char­ acteristic of these suckers-photophores. If the suck­ ers were then to develop a bio luminescent capac­ ity, the effeCt w ould be funher amplified, resulting in an immediate selecti,·e ad\-antage for the light emitter. Many bioluminescent animals exhibit multiple uses of light emission, which is undoubtedly a conse­ quence of multiple selection pressures. For example, in many cases animals that u e bioluminescence for Fig. 3. Suckers as light organs. (a) Seen under white light, attracting mates or finding food also emit light de­ the suckers-photophores of the octopus Stauroteuthis syrtensis appear highly reflective. (b) In the dark these fensively. Since captured specimens of S. syrt en sis same structures emit blue light. (Photos by E. Widder/ were observed to emiLli ght when disturbed, it may Harbor Branch Oceanog. © 1999) Biomining 55

s. syrtensis and the incirrates j apetella and biomining microorganisms causes disease in plants, £/edonella), it is interesting that they occur in such animals, or h umans. dissimilar suborders (the Cirrata and lncirrata) with There are three distinct groups of biomining o r­ rwo such different forms ofexpress ion . \Vhile the cir­ ganisms: (1) mesophilic bacteria that live and repro­ rates have fins and cirri (two thin armlike projections duce at about 50- 110~ (10-45°C); (2) moderately associated w ith each sucker), the incirrates have nei­ thermophilic (beat-loving) bacteria that function at ther. The primary similarity between these disparate about 110-140~ (45-60°C).; and (3) extremely ther­ octopods appears tO be their pelagic existence. Be­ mophilic archaea, which gro\v in the 1 40- 1 95~ (60- cause morphology alone is no t an adequate indica­ 900C) temperature range; the archaea are not bacte­ tor of bioluminescence potential, it is necessary to ria, but are life-forms representing one of the earliest observe light emission from putative light organs. living inhabitants on Earth. Such observations require access to healthy spec­ Mescphilic bacteria. Well-studied mesophilic biomin­ imens. Unfortunately, most deep-sea octopods are ing bacteria are Tbiobacillus ferrooxidans (rod­ collected w ith nets and are usually brough t up dead. sh aped) and Leptospirillum ferroo.:'Cidans (cw-ved­ Perhaps, with greater access to the deep oceans with rod-sbaped); both are 0.5 micrometer in diamete r submersibles, unmanned vehicles, and long-term by 1.0-2.0 J.Lm long. To obtain suf.ficient energy for observatories, new instances of bioluminescence in growth and reproduction, these bacteria oxidize octopods will be discovered . prodigious amounts of ferrous iron. Tbiobacillus For background information see BI OL~ Jbiooxidans, which oxidize elemental sulfur to sul­ CENCE; CEPIW.OPODA; DEEP-SEA FAUNA; OCTOPUS; furic acid, are also mesophilic bacteria of commer­ ORGANIC EVOLUTION in the McGraw-Hill Encyclope­ dal importance. Tbiobacillus and Leptospirillum dia of Science & Technology. Edith A. Widder spedes are found worldwide and are especially Bibliography. S. Johnsen et al., Bioluminescence in abundant in and around acid springs, volcanic re­ the deep-sea cirrate octopod Stauroteutbis syrtensis gions, locales with sulfur mineralization, biomining Verrill (Mollusca: Cephalopoda), Bioi. Bull., 197:26- operations, and some soils. 39, 1999; S. Johnsen, E. ). Balser, and E. A. Widder, Thennophilic bacteria Moderately thermophilic bacte­ light-emitting suckers in an octopus, Nature, 398: ria are less studied than mesophilic bacteria, and 113-114, 1999; B. H. Ro bison and R. E. Young, Bio­ many are yet to be named. Suifobacillus species ob­ luminescence in pelagic octo pods, Pacif. Sci., 35:39- tain oxygen and carbon dioxide from the atmosphere 44, 1981. to oxidize ferrous iron; some also oxidize elemental sulfur. Moderately thermophilic bacteria are 1 J.Lm in diameter by 5-l 0 J.I.ID long and rod-shaped. The mod- . e.rately thermophilic bacteria are found in the same Biomining types of natural environments as the mesophilic bac­ Biornining uses microorganisms to recover metals teria, becoming more abundant as the temperature of value, -Such as gold, silver, and copper, from sul­ increases. fide minerals. A technically and commercially proven Thermophilic archaea. The most studied extremely process, biomining is acknowledged by the global thermophilic archaea are Suifolobus a cidocaldarius, mining industry as being cost-effective , simple Acidianus_ Orierleyi, and Metallospbaera sedula. to use, robust, less environmentally polluting than There are many others which are yet to be named. smelting or mineral roasting practices, and highly These organisms are 1-2 J.Lm in diameter and spher­ suitable for remote and inaccessible regions of the ical in shape. Archaea have no rigid wall surround­ world. ing the microbial cell like the other biomining Centuries of gold and silver mining have depleted bacteria, but have a membrane covered with an many of the high-grade and easy-to-process deposits amorphous layer. Archaea grow using ferrous iron of precious metals. In remaining ore deposits the and various sulfur substances and obtain oxygen and gold and silver are diluted by large amounts of non­ carbon dioxide from air. The archaea dwell in the valuable rock (low-grade ores), or the precious m et­ harshest conditions on Earth- very hot add springs, als occur in minerals that are no t amenable to low­ volcanic zones, hot coal waste piles, deep oceans cost extractive processes (refractory ores). Bioheap where sulfur gases vent, and h ot biomining opera­ leaching is a simple and cost-effective process that tions. They grow and reproduce in s ulfuric acid en­ applies biorniniog technology to recover gold and "ironments approaching boiling temperatures with silver from low-grade, refractory ores. high dissolved metal content and low amounts of Microorganisms. Biomining microorganisms are oxygen , carbon dioxide, ammonium, and phosphate. unique and robust. They obtain energy for repro­ Metal recovery process. The biomining micro­ duction and growth by oxidizing ferrous iron (Fe2 +), organisms oxidize ferrous iron in a sulfuric acid and 0 elemental sulfur (S ), and certain other sulfur sub­ water (H20) environment to ferric iron (Fe3+) stances. These organism s require oxygen COV and [reaction (1)) . Ferric iron is a strong oxidant that carbon dioxide (COv, obtained from air, and some nitrogen and phosphorus. The biomining organisms need a sulfuric acid (H2S04) environment of pH 2.5 down to a minimum of about pH 0.5. None of the anacks sulfide minerals, causing the minerals to