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Thoughts on the diversity of convergent evolution of bioluminescence on earth

Published online by Cambridge University Press:  02 May 2012

Hans E. Waldenmaier ,
Anderson G. Oliveira  and
Cassius V. Stevani
Hans E. Waldenmaier
Affiliation:
Departamento de Química Fundamental, Instituto de Química, Universidade de São Paulo, CP 26077, 05599-970 São Paulo, SP, Brazil
Anderson G. Oliveira
Affiliation:
Departamento de Genética e Evolução, Universidade Federal de São Carlos, 13500-900, Sorocaba, SP, Brazil
Cassius V. Stevani*
Affiliation:
Departamento de Química Fundamental, Instituto de Química, Universidade de São Paulo, CP 26077, 05599-970 São Paulo, SP, Brazil
*
e-mail: stevani@iq.usp.br
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Abstract

The widespread independent evolution of analogous bioluminescent systems is one of the most impressive and diverse examples of convergent evolution on earth. There are roughly 30 extant bioluminescent systems that have evolved independently on Earth, with each system likely having unique enzymes responsible for catalysing the bioluminescent reaction. Bioluminescence is a chemical reaction involving a luciferin molecule and a luciferase or photoprotein that results in the emission of light. Some independent systems utilize the same luciferin, such as the use of tetrapyrrolic compounds by krill and dinoflagellates, and the wide use of coelenterazine by marine organisms, while the enzymes involved are unique. One common thread among all the different bioluminescent systems is the requirement of molecular oxygen. Bioluminescence is found in most forms of life, especially marine organisms.

Bioluminescence in known to benefit the organism by: attraction, repulsion, communication, camouflage, and illumination. The marine ecosystem is significantly affected by bioluminescence, the only light found in the pelagic zone and below is from bioluminescent organisms.

Transgenic bioluminescent organisms have revolutionized molecular research, medicine and the biotechnology industry. The use of bioluminescence in studying molecular pathways and disease allows for non-invasive and real-time analysis. Bioluminescence-based assays have been developed for several analytes by coupling luminescence to many enzyme-catalysed reactions.

Keywords

bioluminescencedioxetanoneLuciferaseluciferinphotoproteins

Information

Type
Research Article
Information
International Journal of Astrobiology , Volume 11 , Issue 4: SPECIAL ISSUE: THE SAO PAULO ADVANCED SCHOOL OF ASTROBIOLOGY – SPASA 2011 , October 2012 , pp. 335 - 343
Copyright
Copyright © Cambridge University Press 2012

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References

Abrahams, M.V. & Townsend, L.D. (1993). Bioluminescence in Dinoglagellates: a test of the burglar alarm hypothesis. Ecology 74(1), 258–260.Google Scholar
Airth, R.L. & Foerster, G.E. (1962). The isolation of catalytic components required for cell-free fungal bioluminescence. Arch. Biochm. Biophys. 92, 567–573.Google Scholar
Airth, R.L. & McElroy, W.D. (1959). Light emission from extracts of luminous fungi. J. Bacteriol. 77, 249–250.Google Scholar
Bae, Y.M. & Hastings, J.W. (1994). Cloning, sequencing and expresssion of dinoflagellate luciferase DNA from a marine alga, Gonyaulax polyedra. Biochim. Biophys. Acta 1219, 449–456.Google Scholar
Bellisario, R., Spencer, T.E. & Cormier, M.J. (1972). Isolation and properties of luciferase, a non-heme peroxide from the bioluminescent earthworm, Diplocardia longa. Biochemistry 11, 2256–2266.Google Scholar
Berkel, W.J.H., Kamerbeek, N.M. & Fraaije, M.W. (2006). Favoprotein monooxygenases, a diverse class of oxidative biocatalysts. J. Biotechnol. 124, 670–689.CrossRefGoogle ScholarPubMed
Bowden, B.J. (1950). Some observations on a luminescent freshwater limpet from New Zealand. Biol. Bull. 99, 373–380.Google Scholar
Campbell, A.K. & Herring, P.J. (1990). Imidazopyrazine bioluminescence in copepods and other marine organisms. Mar. Biol. 104, 219–225.Google Scholar
Chalfie, M., Tu, Y., Euskirchen, G. & Ward, W.W. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802–805.Google Scholar
Conti, E., Franks, N.P. & Brick, P. (1996). Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4(3), 287–298.CrossRefGoogle ScholarPubMed
Cormier, M.J. & Strehler, B.L. (1953). The identification of KCF: requirement of long-chain aldehydes for bacterial extract luminescence. Am. Chem. Soc. 75, 4864–4865.Google Scholar
Daunert, S., Barrett, G., Feliciano, J.S., Shetty, R.S., Shrestha, S. & Smith-Spencer, W. (2000). Genetically engineered whole-cell sensing systems: coupling biological recognition with reporter genes. Chem. Rev. 100, 2705–2738.CrossRefGoogle ScholarPubMed
Deheyn, D.D. & Latz, M.I. (2009). Internal and secreted bioluminescence of the marine polychaete Odontosyllis phosphorea (Syllidae). Invertebr. Biol. 128(1), 31–45.Google Scholar
Desjardin, D.E., Oliveira, A.G. & Stevani, C.V. (2008). Fungi bioluminescence revisited. Photochem. Photobiol. Sci. 7, 170–182.Google Scholar
Desjardin, D.E., Perry, B.A., Lodge, D.J., Stevani, C.V. & Nagasawa, E. (2010). Luminescent Mycena: new and noteworthy species. Mycologia. 102, 459–477.CrossRefGoogle ScholarPubMed
Dragulescu-Andrasi, A., Chan, C.T., De, A., Massoud, T.F. & Gambhir, S.S. (2011). Bioluminescence resonance energy transfer (BRET) imaging of protein–protein interactions within deep tissues of living subjects. Proc. Natl. Acad. Sci. U.S.A. 108(29), 12060–12065.Google Scholar
Dunlap, J.C., Hastings, J.W. & Shimomura, O. (1980). Crossreactivity between the light-emitting systems of distantly related organisms: novel type of light-emitting compound. Proc. Natl. Acad. Sci. U.S.A. 77, 1394–1397.Google Scholar
Eckstein, J.W., Hastings, J.W. & Ghisla, S. (1993). Mechanism of bacterial bioluminescence: 4a,5-dihydroflavin analogs as models for luciferase hydroperoxide intermediates and the effect of substituents at the 8-position of flavin on luciferase kinetics. Biochemistry 32, 404–411.Google Scholar
Fairey, E.R. & Ramsdell, J.S. (1999). Reporter gene assays for algal-derived toxins. Nat. Toxins 7, 415–421.3.0.CO;2-E>CrossRefGoogle ScholarPubMed
Francis, K.P., Joh, D., Bellinger-Kawahara, C., Hawkinson, M.J., Purchio, T.F. & Contag, P.R. (2000). Monitoring bioluminescent Staphylococcus aureus infections in living mice using a novel luxABCDE construct. Infect. Immun. 68, 3594–3600.Google Scholar
Gatenby, J.B. (1959). Notes on the New Zealand Glow-worm, Bolitophila (Arachnocampa) luminosa. Trans. R. Soc. N. Z. 87, 291–314.Google Scholar
Germain-Desprez, D., Bazinet, M., Bouvier, M. & Aubry, M. (2003). Oligomerization of transcriptional intermediary factor 1 regulators and interaction with ZNF74 nuclear matrix protein revealed by bioluminescence resonance energy transfer in living cells. J. Biol. Chem. 278(25), 22367–22373.Google Scholar
Harvey, E.N. (1952). Bioluminescence. Academic Press, New York.Google Scholar
Issad, T., Boute, N. & Pernet, K. (2002). A homogeneous assay to monitor the acivity of the insulin receptor using bioluminescence resonance energy transfer. Biochem. Pharmacol. 64, 813–817.Google Scholar
Kenaley, C.P. (2010). Comparative innervation of Cephalic photophores of the loosejaw dragonfishes (Teleostei: Stomiiformes: Stomiidae): evidence for parallel evolution of long-wave bioluminescence. J. Morphol. 271, 418–437.CrossRefGoogle ScholarPubMed
Kishi, Y., Goto, T. & Hirata, Y. (1966). Cypridina bioluminescence I: structure of Cypridina luciferin. Tetrahedron Lett. 29, 3427–3436.Google Scholar
Kojima, S. et al. (2000). Purification and characterization of the luciferase from the freshwater snail Latia. In Abstracts of 11th International Symposium on Bioluminescence and Chemiluminescence, Asilomar, CA, p. 57.Google Scholar
Liu, Y., Cotton, J.A., Shen, B., Han, X., Rossiter, S.J. & Zhang, S. (2010). Convergent sequence evolution between echolocating bats and dolphins. Curr. Biol. 20, R53–54.Google Scholar
Meighen, E.A. (1991). Molecular biology of bacterial bioluminescence. Microbiol. Mol. Biol. Rev. 55(1), 123–141.Google ScholarPubMed
Meighen, E.A. (1994). Genetics of bacterial bioluminescence. Annu. Rev. Genet. 28, 117–139.Google Scholar
Mitchell, R.J. & Gu, M.B. (2003). An Escherichia coli biosensor capable of detecting both genotoxic and oxidative damage. Appl. Microbiol. Biotechnol. 64, 46–52.Google Scholar
Morin, J.G. (1983). Coastal bioluminescence: patterns and functions. Bull. Mar. Sci. 33, 787–817.Google Scholar
Morise, H., Shimomura, O., Johnson, F. H., & Winant, J. (1974). Intermolecular energy transfer in the bioluminescent system of Aequorea. Biochemistry 13, 2656–2662.Google Scholar
Nakajima, Y., Kobayashi, K., Yamagishi, K., Entomoto, T. & Ohmiya, Y. (2004). cDNA cloning and characterization of a secreted luciferase from the luminous Japanese ostracod, Cypridina noctiluca. Biosci. Biotechnol. Biochem. 68, 565–570.CrossRefGoogle ScholarPubMed
Nakamura, H., Musicki, B., Kishi, Y. & Shimomura, O. (1988). Structure of the light emitter in krill Euphausia pacifica. J. Am. Chem. Soc. 110, 2683–2685.Google Scholar
Nakamura, H., Kishi, Y., Shimomura, O., Morse, D. & Hastings, J.W. (1989). Structure of dinoflagellate luciferin and its enzymatic and nonenzymatic air-oxidation products. J. Am. Chem. Soc. 111, 7607–7611.CrossRefGoogle Scholar
Ohtsuka, H., Rudie, N.G. & Wampler, J.E. (1976). Structural identification and synthesis of luciferin from the bioluminescent earthworm, Diplocardia longa. Biochemistry 15, 1001–1004.Google Scholar
Oliveira, A.G. & Stevani, C.V. (2009). The enzymatic nature of fungal bioluminescence. Photochem. Photobiol. Sci. 8, 1416–1421.Google Scholar
Oliveira, A.G., Desjardin, D.E., Perry, B.A. & Stevani, C.V. (2012). Evidence that a single bioluminescent system is shared by all known bioluminescent fungal lineages. Photochem. Photobiol. Sci. DOI: 10.1039/C2PP25032B.Google Scholar
Ow, D.W., Wood, K.V., DeLuca, M., De Wet, J.R., Helinski, D.R. & Howell, S.H. (1986). Transient and stable expression of the firefly luciferase gene in plant cells and transgenic plants. Science 234, 856–859.Google Scholar
Roda, A., Girotti, S., Grigolo, B., Ghini, S., Carrea, G., Bovara, R., Zini, I. & Grimaldi, R. (1991). Microdialysis and luminescent probe: analytical and clinical aspects. Biosens. Bioelectron. 6, 21–29.Google Scholar
Roda, A., Pasini, P., Mirasoli, M., Michelini, E. & Guardigli, M. (2004). Biotechnological applications of bioluminescence and chemiluminescence. Trends Biotechnol. 22, 295–303.CrossRefGoogle ScholarPubMed
Rudie, N.G., Mulkerrin, M.G. & Wampler, J.E. (1981). Earthworm bioluminescence: characterization of high specific activity Diplocardia longa luciferase and the reaction it catalyzes. Biochemistry 20, 344–350.Google Scholar
Schultz, L.W., Lie, L., Cegielski, M. & Hastings, J.W. (2005). Crystal structure of a pH-regulated luciferase catalyzing the bioluminescent oxidation of an open tetrapyrrole. Proc. Natl. Acad. Sci. U.S.A. 102, 1378–1383.CrossRefGoogle ScholarPubMed
Seliger, H.H. & McElroy, W.D. (1964). The colors of firefly bioluminescence: enzyme configuration and species specificity. Proc. Natl. Acad. Sci. U.S.A. 52, 75–81.CrossRefGoogle ScholarPubMed
Shimomura, O. (1979). Structure of the chromophore of Aequorea green fluorescent protein. FEBS Lett. 104, 220–222.Google Scholar
Shimomura, O. (1995). The roles of the two highly unstable components F and P involved in the bioluminescence of euphausiid shrimps. J. Biolumin. Chemilumin. 10, 91–101.Google Scholar
Shimomura, O. (2006). Bioluminescence: Chemical Principles and Methods. World Scientific, Singapore.Google Scholar
Shimomura, O. & Johnson, F.H. (1968a). The structure of Latia luciferin. Biochemistry 7, 1734–1738.Google Scholar
Shimomura, O. & Johnson, F.H. (1968b). Purification and properties of the luciferase and of a protein cofactor in the bioluminescence system of Latia neritoides. Biochemistry 7, 2574–2580.CrossRefGoogle ScholarPubMed
Shimomura, O. & Johnson, F.H. (1970). Mechanisms in the quantum yield of Cypridina bioluminescence. Photochem, Photobiol. 12, 291–295.Google Scholar
Shimomura, O. & Johnson, F.H. (1971). Mechanism of the luminescent oxidation of Cypridina luciferin. Biochem. Biophys. Res. Commun. 44, 340–346.Google Scholar
Shimomura, O., Johnson, F.H. & Saiga, Y. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, aequorea. J. Cell. Comp. Physiol. 59, 223–239.Google Scholar
Shimomura, O., Goto, T. & Johnson, F.H. (1977). Source of oxygen in the CO2 produced in the bioluminescent oxidation of firefly luciferin. Proc. Natl. Acad. Sci. U.S.A. 74, 2799–2802.Google Scholar
Siewers, V., Smedsgaard, J. & Tudzynski, P. (2004). The P450 monooxygenase BcABA1 is essential for abscisic acid biosynthesis in Botrytis cinerea. Appl Environ. Microbiol. 70(7), 3868–3876.CrossRefGoogle ScholarPubMed
Sivinski, J. (1981). Arthropods attracted to luminous fungi. Psyche 88, 383–390.CrossRefGoogle Scholar
Sivinski, J. (1998). Phototrophism, bioluminescence, and the diptera. Florida Entomol. 81(3), 282–292.Google Scholar
Stevani, C.V. & Baader, W.J. (1999). O sistema quimiluminescente peróxi-oxalato. Quim. Nova 22, 715–723.Google Scholar
Stojanovic, M.N. & Kishi, Y. (1994). Dinoflagellate bioluminescence: the chemical behavior of the chromophore towards oxidants. Tetrahedron Lett. 35, 9347–9350.CrossRefGoogle Scholar
Szent-Gyorgyi, C., Ballou, B.T., Dagnal, E. & Bryan, B. (1999). Cloning and characterization of new bioluminescent proteins. In Proceedings of SPIE-The International Society for Optical Engineering (Biomedical Imaging: Reporters, Dyes, and Instrumentation), p. 4.Google Scholar
Sutton, T.T. (2005). Trophic ecology of the deep-sea fish Malacosteus niger (Pisces: Stomiidae): an enigmatic feeding ecology to facilitate a unique visual system. Deep Sea Res. 52, 2065–2076.Google Scholar
Thompson, E.M., Nagata, S. & Tsuji, F.I. (1989). Cloning and expression of cDNA for the luciferase from the marine ostracod Vargulahilgendorfii. Proc. Natl. Acad. Sci. U.S.A. 86, 6567–6571.CrossRefGoogle Scholar
Trezzani, I., Nadir, M., Dorel, C., Lejeune, P., Bellalou, J., Lieto, J., Hammouri, H., Longin, R. & Dhurjati, P. (2003). Monitoring of recombinant protein production using bioluminescence in a semiautomated fermentation process. Biotechnol. Prog. 19, 1377–1382.Google Scholar
Tu, S.C. (2007). Activity coupling and complex formation between bacterial luciferase and flavin reductases. Photochem. Photobiol. Sci. 7, 183–188.Google Scholar
Tudzynski, B. (2005). Gibberellin biosynthesis in fungi: genes, enzymes, evolution, and impact on biotechnology. Appl. Microbiol. Biotechnol. 66(6), 597–611.Google Scholar
Villa, R. & Willetts, A. (1997). Oxidations by microbial NADH plus FMN-dependent luciferases from Photobacterium phosphoreum and Vibrio fischeri. J. Mol. Catal. 2, 193–197.Google Scholar
Viviani, V.R. (2002). The origin, diversity, and structure function relationships of insect luciferases. Cell. Mol. Life Sci.. 59, 1833–1850.Google Scholar
Viviani, V.R., Silva, A.C.R., Perez, G.L.O., Santelli, R.V., Bechara, E.J.H. & Reinach, F.C. (1999). Cloning and molecular characterization of the cDNA for the Brazilian larval ciick-beetle Pyrearinus termitilluminans luciferase. Photochem. Photobiol. 70, 254–260.Google Scholar
Watanabe, H. & Hastings, J.W. (1982). Specificities and properties of three reducted pyridine nucleotide-flavin mononucleotide reductases coupling to bacterial luciferase. Mol. Cell Biochem. 44, 181–187.Google Scholar
White, E.H., McCapra, F., Field, G. & McElroy, W.D. (1961). The structure and synthesis of firefly luciferin. J. Am. Chem. Soc. 83, 2402–2403.CrossRefGoogle Scholar
Widder, E.A. (2001). Bioluminescence and the Pelagic visual environment. Mar. Fresh. Behav. Physiol. 35, 1–26.CrossRefGoogle Scholar
Wilson, T. & Hastings, J.W. (1998). Bioluminescence. Annu. Rev. Dev. Biol. 14, 197–230.Google Scholar
Wood, K.V., De Wet, J.R., Dewji, N. & DeLuca, M. (1984). Synthesis of active firefly luciferase by in vitro translation of RNA obtained from adult lanterns. Biochem. Biophys. Res. Commun. 124, 592–596.Google Scholar
Wood, K.V., Lam, Y.A., Seliger, H.H. & McElroy, W.D. (1989). Complementary DNA coding click beetle luciferase can elicit bioluminescence of different colors. Science 244, 700–702.Google Scholar
Wu, J.C., Chen, I.Y., Sundaresan, G., Min, J.J., De, A., Qiao, J.H., Fishbein, M.C. & Gambhir, S.S. (2003). Molecular imaging of cardiac cell transplantation in living animals using optical bioluminescence and positron emission tomography. Circulation 108, 1302–1305.Google Scholar
Yu, Y.A., Timiryasova, T., Zhang, Q., Beltz, R. & Szalay, A.A. (2003). Optical imaging: bacteria, viruses, and mammalian cells encoding light-emitting proteins reveal the locations of primary tumors and metastases in animals. Anal. Bioanal. Chem. 377, 964–972.Google Scholar
Zenno, S. & Saigo, K. (1994). Identification of the genes encoding NAD(P)H flavin oxidoreductases that are similar in sequence to Escherichia coli Fre in four species of luminous bacteria Photohabdus luminescens, Vibrio fischeri, vibrio harveyi and vibrio orientalis. J. Bacteriol 176, 3544–3551.Google Scholar
Zhang, W., Purchio, A.F., Chen, K., Wu, J., Lu, L., Coffee, R., Contag, P.R. & West, D.B. (2003). A transgenic mouse model with a luciferase reporter for studying in vivo transcriptional regulation of the human CYP3A4 gene. Drug Metab. Dispos. 31, 1054–1064.Google Scholar