ON THE ORIGIN OF BIOLUMINESCENT SYSTEMS
Y. A. LABAS
Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky Prospect
33, 117071 Moscow, Russia
Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya
16/10, 117871 Moscow, Russia
Center for Craniofacial Molecular Biology, University of Southern California,
2250 Alcazar Street, CSA 103, Los Angeles, CA 90033, USA
1. THE PROBLEM OF GLOWING MUTATIONS
Bioluminescent systems (BS) are present in aerobic organisms on different levels
of phylogenesis from bacteria to fishes. There are no bioluminescent species
among autotrophs (except dinoflagellates), some groups of sea invertebrates
and terrestrial animals, and for unknown reason - in fresh water organisms (exception
- gastropodа Latia neritoides and some species of parasitic photobacteria).1
Charles Darwin has mentioned that the origin of the bioluminescence is the
problematic questions in his theory.2 The function of the bioluminescence has
a direct connection with the vision behavior of the organisms. It could be chasing
the predators with flashes, camouflage, communication, and attraction with steady
glowing (fungi non-symbiotic photobacteria).3-5 It means that the initial material
for evolution were only such neutral mutations of non-luminescent organisms
which resulted in well visible glowing, connected with certain behavior reactions
in impulse mode (e.g. escape). It suggests preexistence in non-bioluminescent
precursor species of all major components of the BS: luciferin (L), luciferase
(E) or their analogs, and triggering mechanisms and secondary emitters (GFPs
from coelenterates, blue fluorescent proteins from photobacteria, red fluorescent
protein from deep-sea fish Malacosteus niger). Different phyla have different
L and E. Taking in account dissimilariti between L,E and other components of
BS-s in different phyla, it is reasonable to suppose that about 30 types of
its were originated indepedently from preexisting nonbioluminescent reactions.6
There are some reports on conditionally bioluminescent species. In some non-bioluminescent
species of Copepoda, e.g. Nannocalanus minor and Oithona plumifera occasionally
could be found specimens which use to glow under stimulation.7 There are both
luminous and non-luminous species in one genera: e.g. Obelia - among Hydrozoa,8
Oncaea, Oithona, among Cyclopodia.7 The close taxonomic relations of luminous
species with non-luminous is evidence in favor of the recent genesis of some
BS via light-emitting neutral mutations in non bioluminescent organisms.
2. THE PROBLEM OF ANCESTRAL FUNCTION
There are many evidence that an ancestral function of L and some E was detoxification
of reactive oxygen species (ROS), based on the antioxidant abilities of L.5,9-11
Coelenterazine occurs in many luminous marine species as well as in non-luminescent
species.12 Some L are able to emit light with ROS in the absence of E.13-15
The luminescence of E-L photoprotein complexes also could be activated by ROS
but not by molecular oxygen in Pholas dactylus,16 and in Polynoinae which have
a specific reaction for superoxide.17 The calcium-activated photoprotein obelin
is able to emit light in absence of calcium but in the presence of singlet oxygen.18
An activation of Е synthesis аs well as antioxidant enzymes such as SOD and
catalase during hyperoxygenation may be an indication of the antioxidant origination
of E in fireflies.10 Bacterial E is able to give a luminescent reaction in vitro
in the presence of H2O2 or other ROS and in the absence of aliphatic aldehyde.11
In some eukaryotes an impulse luminescent flash initiates an endogenous release
of ROS - e.g. in earthworms Diplocardia longa and ascidians Clavelina miniata
BS is localized in phagocytes - “cells of the respiratory burst”.19,20. The
content of those phagocytes in D.longa use to glow in the fluided exuded in
the presence of endogenous H2O2. In non-bioluminescent earthworm Lampito mauritii
phagocytes also use to glow in the presence of H2O2.21 In Polynoinae intracellular
luminescence is the result of enzymatic generation of superoxide.17 . There
are another mechanisms of bioluminescence triggering in Dinoflagellata through
H+ or calcium in Anthozoa with an induced release of L from the complex with
luciferin-binding protein (LBP).22,23 Based on this data we suggest here that
an ancestral function of the L and some E could be the protection of the cells
from the ROS which used to be secreted by those prophotogenic cells. In some
bioluminescent eukaryotes it happens in impulse mode. The original function
of LBP could be the protection of antioxidants - proluciferins from the self-oxidation
prior the respiratory burst. The generation of ROS in low concentration is one
of the necessary conditions for the normal physiology (functions of the secondary
messengers, defense or offense, etc). An absence of BS in freshwater organisms
could be explained by fact that many BS were the scavengers of HOCl- ion that
could be the terminal product in ROS secretion only at the high concentration
of Cl- ion in the environment. Anthozoa and Hydrozoa have different types of
E and relatively close GFPs and L. It means that their BS have originated independently
whereas GFPs and L were inherited from a common non-bioluminescent ancestor.
Prediction of that fact resulted in a discovery of a new family of GFP-like
proteins in non-bioluminescent Anthozoa.25 We also suggest that photocytes in
Anthozoa originated from an entodermal pigment cells which able to secrete ROS
for phagocytosis. Supposed function of GFP-like proteins could be photoactivation
of enzyme reactions and tissue photoreception.
[Supported by Russian Foundation for Fundamental research (grant 99-04-48873)].
1. Harvey EN. Bioluminescence. New York: Academic Press, 1952: 542.
2. Darwin CR. The origin of species by means of natural selection. London:
John Murray, 1859: 502.
3. Hastings JW. Bioluminescence. In: Speralakis N, ed. Cell Physiology. New
York: Academic Press, 1995: 651-681.
4. Sivinski JM. Phototropism, bioluminescence, and the Diptera. Florida Entomologist
1998; 81: 282-292.
5. Wilson T, Hastings JW. Bioluminescence. Annu Rev Cell Dev Biol 1998; 14:
6. Buck JB. Function and evolution of bioluminescence. In: Herring PJ, ed.
Bioluminescence in Action. London: Academic Press, 1978: 419-460.
7. Evstigneev PV, Bitjukov EP. Bioluminescencija morskich copepod. Kiev: Naukova
dumka, 1990: 145.
8. Morin JG. Coelenterate bioluminescence. In: Muscatine L, Lenhoff H, eds.
Coelenterates Biology. Review of New Perspectives. New York: Academic Press,
9. Rees JF, de Wergifoss B, Noiset O, Dubuisson M, Janssens B, Thompson EM.
The origins of marine bioluminescence: turning oxygen defense mechanisms into
deep-sea communication tools. J Exp Biol 1998; 201: 1211-1221.
10. Barros MP, Bechara EJ. Bioluminescence as a possible auxiliary oxygen
detoxifying mechanism in elaterid larvae. Free Radic Biol Med 1998; 24: 767-777.
11. Watanabe H, Nagoshi T, Inaba, H. Luminescence of bacterial luciferase
intermediate by reaction with H2O2: The evolutionary origin of luciferase and
source of endogenous light-emission. Biochem Biophys Acta 1993; 1141: 297-302.
12. Thompson CM, Herring PJ, Campbell AK. The widespread occurrence and tissue
distribution of the imidazolopyrazine luciferins. J Biolumin Chemilumin 1997;
13. Skatchkov MP, Sperling D, Hink U, Anggard E, Munzel T. Quantification
of superoxide radical formation in intact vascular tissue using a Cypridina
luciferin analog as an alternative to lucigenin. Biochem Biophys Res Commun
1998; 248: 382-386.
14. Akutsu K, Nakajima H, Katoh T, Kino S, Fujimori K. Chemiluminescence of
Cipridina luciferin analogs. 2. Kinetic studies on the reaction of 2-methyl-6-phenylimidazo(1,2-a)pyrazin-3(7H)-one(CLA)
with superoxide-hydroperoxyl radical is an actual active species used in initiate
the reaction. J Chem Soc - Perkin Trans 1995; 2: 1699-1706.
15. Shimomura O. Superoxide triggered chemiluminescence of the extract of
luminous mushroom Pannelus stripticus after treatment with methylamine. J Exp
Bot 1991; 41: 555-560.
16. Roberts PA, Knight J, Campbell AK. Pholasin--a bioluminescent indicator
for detecting activation of single neutrophils. Anal Biochem 1987; 160: 139-148.
17. Bassot JM, Nicolas MT. Bioluminescence in scale-worm photosomes: the photoprotein
polynoidin is specific for the detection of superoxide radicals. Histochem Cell
Biol 1995; 104: 199-210.
18. Vysotsky ES, Trofimov KP, Bondar VS, Gitelson JJ. Luminescence of Ca2+-activated
photoprotein obelin iniciated by NaOCl and MnCl2. J Biolumin Chemilumin 1993;
19. Belissario R, Spencer TE, Cormier MJ. Isolation and properties of luciferase,
a non-heme peroxidase from the bioluminescent earthworm, Diplocardia longa.
Biochemistry 1972; 11: 2256-2266.
20. Chiba K.,Hoshi M.,Isobe M.,Hirose E.Bioluminescence in the tunic of the
colonial ascidian, Clavelina miniata: identification of luminous cells in vitro.
J.of Exper.Zool.1998. 281:546-553
21. Sanhanam KSV, Limaye NM. Electrobioluminescence of cells extracted from
Lampito mauritii. Biochem Bioenerg 1989; 22: 219-229.
22. Lee DH, Mittag M, Sczekan S, Morse D, Hastings JW. Molecular cloning and
genomic organization of a gene for luciferin-binding protein from the dinoflagellate
Gonyaulax polyedra. J Biol Chem 1993; 268: 8842-8850.
23. Anderson JM, Carbonneau H, Cormier MJ. Mechanism of calcium induction
of Renilla bioluminescence. Involvement of calcium-trigged luciferin binding
protein. Biochemistry 1974; 13: 1195-1200.
24. Kumar S, Harrylock M, Walsh KA, Cormier MJ, Charbonneau H. Amino acid
sequence of the Ca2(+)-triggered luciferin binding protein of Renilla reniformis.
FEBS Letters 1990; 268: 287-290.
25. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AZ, Markelov ML,
Lukyanov SA. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat
Biotech 1999; 17: 969-973.
PROC. OF THE 11 INTERN. SYMPOSIUM ON BIOLUMINESCENCE AND
CASE J.F., HERRING P.J.,ROBINSON B.F.,HADDOCK S.H.D.,KRICKA L.J.,STANLEY