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Current Biology

Magazine

faces — whereby individual features Quick guide from violet and blue (420–500 nm) in
are integrated into a coherent unified the deep sea to blue-green (460–520
whole — compromising the accuracy
and efficiency of their face recognition.
Bioluminescence nm) in shallow waters to green-yellow
(520–580 nm) on land, and its hue
Neuroimaging studies have revealed is often correlated with the optical
subtle neuroanatomical differences Tim Kahlke1,* and Kate D.L. Umbers2
characteristics of the environment
that accompany the condition. Several (Figure 1D). The color of the
regions of the visual brain known to play What is bioluminescence? bioluminescent light is dependent on
an important role in face recognition, Bioluminescence is the emission of multiple factors such as the luciferins
including the fusiform and occipital face light by an organism as a result of a and luciferases that are involved
areas, appear to be under-connected in biochemical reaction. In contrast to in the bioluminescent reaction or
developmental prosopagnosia, possibly fluorescence and phosphorescence, the conformation of the luciferase.
impairing information exchange within bioluminescence reactions do not In some bioluminescent systems
this network. In particular, the integrity require the initial absorption of fluorescent pigments, e.g. the green
of the inferior longitudinal fasciculus, sunlight or other electromagnetic fluorescent protein (GFP), act as
a white matter tract connecting the radiation by a molecule or pigment to secondary emitters that affect the
occipital and temporal lobes, is reduced emit light. Bioluminescent systems emitted color of the light. In addition
in many developmental prosopagnosics produce light through the oxygenation to variations of the light-emitting
(Figure 1). of a substrate, generically called molecules some organisms alter the
luciferin (lat. lucifer, the light- original color of the bioluminescence
Is developmental prosopagnosia bringer), and an enzyme, luciferase. through anatomical structures that act
related to autism? Developmental Bioluminescent reactions vary as biological filters and can refract or
prosopagnosia may be more common greatly among organisms but can reflect the emitted light.
in individuals with autism spectrum generally be described as a luciferase
disorder than in the general population. catalyzed production of an excited How is bioluminescence
Importantly, however, the two conditions intermediate from oxygen and luciferin distributed among taxa? To
are independent; many individuals that emits light when returning to date, bioluminescence has been
develop autism spectrum disorder in the its ground state. Additionally, many reported in nearly 700 prokaryotic
absence of face recognition difficulties, bioluminescence systems involve and eukaryotic genera. The majority
and many prosopagnosics exhibit cofactors such as FMNH2, ATP, of bioluminescent organisms
no signs of autistic symptomology. additional enzymes and intermediate inhabit marine environments
Developmental prosopagnosia is an steps for the light production (Figure including bacteria, dinoflagellates
example of a ‘neurodevelopmental’ 1E). In some bioluminescence (the well-known ocean glow),
condition, similar to dyslexia, dyspraxia, systems special types of luciferases, molluscs, crustaceans, bony fish
dyscalculia, and autism spectrum photoproteins, bind and stabilize and sharks. In contrast to marine
disorder. Many neurodevelopmental the oxygenated luciferin and emit species, bioluminescence has not
disorders are known to co-occur. light only in the presence of cations, been confirmed in any fresh water
Genetic or environmental factors such as Mg2+ or Ca2+, which acts organisms. On land, bioluminescence
that cause an individual to develop a as a mechanism for the host to is less common and almost
neurodevelopmental condition, such as precisely control the timing of the light exclusively found in fungi and animals.
developmental prosopagnosia, appear emission. Approximately 70 species of fungi in
to increase their chances of developing four lineages of the order Agaricales
others. How does bioluminescent light are bioluminescent. In animals,
differ among organisms? Light bioluminescence has been reported in
Where can I find out more? production in bioluminescence has two phyla, Nematoda and Arthropoda.
Behrmann, M., and Avidan, G. (2005). Congenital
prosopagnosia: face-blind from birth. Trends
a remarkable range of emission Phylum Arthropoda includes one of
Cogn. Sci. 9, 180–187. patterns such as continuous glow the best-known groups of terrestrial
Shah, P., Gaule, A., Sowden, S., Bird, G., and Cook, (Figure 1A,C), single flashes of light, bioluminescent organisms, the fireflies
R. (2015). The 20-item prosopagnosia index
(PI20): a self-report instrument for identifying e.g. in dinoflagellates, or repetitive (order: Coleoptera).
developmental prosopagnosia. R. Soc. Open Sci. pulse patterns that are often species-
2, 140343.
Susilo, T., and Duchaine, B. (2013). Advances in
specific (Figure 1B). Bioluminescent How diverse are bioluminescence
developmental prosopagnosia research. Curr light is emitted in wavelengths systems and what are their
Opin. Neurobiol. 23, 423–429. between 400 and 720 nm, from violet evolutionary origins? Bioluminescent
Thomas, C., Avidan, G., Humphreys, K., Jung, K.J.,
Gao, F., and Behrmann, M. (2009). Reduced into the near-infrared. The majority systems are as diverse as their host
structural connectivity in ventral visual cortex in of bioluminescent marine organisms organisms. Few bioluminescence
congenital prosopagnosia. Nat. Neurosci. 12,
29–31.
emit blue light (410–550 nm), which systems are conserved among related
correlates with the peak sensitivities taxa with the exception of fungi which
Social Perception Research Group, Department of the opsins of many marine are thought to share one conserved
of Psychology, City University London, Whiskin organisms. Interestingly, wavelengths bioluminescence system. Generally,
Street, London EC1R 0JD, UK. of bioluminescent light seem to shift luciferins are more widely conserved
*E-mail: [email protected] based on the habitat of the organism: than luciferases. For example, the

Current Biology 26, R307–R318, April 25, 2016 R313


Current Biology

Magazine

A B C mechanisms through dazzling


predators, aposematism (warning
colouration), prey luring and
courtship. However, outside of
animal taxa, the possible functions
of bioluminescence are less clear,
e.g. in bioluminescent bacteria, or in
fungi that only possess luminescent
mycelium. For bacteria one
D hypothesis is that bioluminescence
150
promotes beneficial interactions
Terrestrial with host organisms as several
Marine - Shallow water bioluminescent bacteria are found
Number of species

Marine - Deep sea


100 Marine - Benthic as symbionts in the light organs of
organisms that lack the ability to emit
light themselves. For example, the
Hawaiian bobtail squid Euprymnia
50
scolopes has a symbiotic relationship
with the bioluminescent bacterium
Vibrio fischerii, which populates
the squid’s light organ. Another
hypothesis is that bioluminescence
400 420 440 460 480 500 520 540 560 580 600 620 640 660 680 700 720 may be incidental in some organisms
Wavelength in nm and that the emission of light is
merely a byproduct of another
E hv essential metabolic function.
+ +
However, the repeated evolution
NAD(P)H/H NAD(P)
O2 of bioluminescence suggests that
Luciferin Luciferin Oxyluciferin + H2O it may directly or indirectly provide
Reductase Luciferase
(reduced) its producer with a selective
Current Biology
advantage over its non-luminescent
counterparts.
Figure 1. Bioluminescence patterns and distribution among different species.
(A) Continuously green (max 530 nm) glowing fungus Neonothopanus gardneri. Photo from
http://www.cell.com/current-biology/fulltext/S0960-9822%2815%2900160-8. (B) Green-
Where can I find out more?
Day, J.C., Tisi, L.C., and Bailey, M.J. (2004).
yellow (max ~550 nm) pulsing light organ of the common glowworm (Lampyris noctiluca). Evolution of beetle bioluminescence: the origin
Image: wikimedia commons. (C) Glowing light organ of a dragonfish Photostomias guernei of beetle luciferin. Luminescence 19, 8–20.
continuously emitting blue (max 530 nm) light. Image: wikimedia commons. (D) Wavelengths Desjardin, D.E., Oliveira, A.G., and Stevani, C.V.
of bioluminescent organisms in different habitats. Number of species are approximated (2008). Fungi bioluminescence revisited.
Photochem. Photobiol. Sci. 7, 170.
for intervals of 20 nm. Redrawn from Widder E.A. (2010). Bioluminescence in the ocean: Dubuisson, M., Marchand, C., and Rees, J.-F.
origins of biological, chemical and ecological diversity. Science 328, 704–708, and Hastings, (2004). Firefly luciferin as antioxidant
J.W. (1996). Chemistries and colors of bioluminescent reactions: a review. Gene 173, 5–11. and light emitter: the evolution of insect
(E) Schematic of the fungal bioluminescence reaction as proposed by Oliveira et al. (2012). bioluminescence. Luminescence 19, 339–344.
Evidence that a single bioluminescent system is shared by all known bioluminescent fungal Haddock, S.H.D., Moline, M.A., and Case, J.F.
(2010). Bioluminescence in the sea. Annu. Rev.
lineages. Photochem. Photobiol Sci. 11, 848. Mar. Sci. 2, 443–493.
Hastings, J.W. (1996). Chemistries and colors of
luciferin coelenterazine is found in hypotheses propose mixed-function bioluminescent reactions: a review. Gene 173,
5–11.
the bioluminescent systems of at oxygenases or, in case of the beetle Stevani, C.V., Oliveira, A.G., Mendes, L.F.,
least nine different marine phyla. In luciferase, certain types of ligases as Ventura, F.F., Waldenmaier, H.E., Carvalho,
R.P., and Pereira, T.A. (2013). Current status
contrast, the luciferases used are the origins of luciferases. of research on fungal bioluminescence:
highly diverse and often species biochemistry and prospects for ecotoxicological
specific. It is currently estimated that What are the ecological functions application. Photochem. Photobiol. 89, 1318–1326.
Viviani, V.R. (2002). The origin, diversity, and
bioluminescence has independently of bioluminescence? Despite structure function relationships of insect
evolved more than 30 times, which the ubiquity of bioluminescence luciferases. Cell. Mol. Life Sci. CMLS 59,
1833–1850.
suggests that the molecular building and the fact that early reports of Widder, E.A. (2010). Bioluminescence in the ocean:
blocks of bioluminescence systems bioluminescence date back to origins of biological, chemical and ecological
are ubiquitous. Nevertheless, ancient Greece (Aristotle, 384–322 diversity. Science 328, 704–708.

their evolutionary origins remain BC and Pliny the Elder, 23–79 AC),
1
mysterious. One hypothesis is that evidence for its ecological functions CSIRO Marine and Atmospheric Research,
Castray Esplanade, Hobart, TAS, Australia.
bioluminescence evolved from is scarce. Suggested functions of 2
School of Science and Health,
detoxification systems as some bioluminescence in organisms are Western Sydney University Hawkesbury,
luciferins show characteristics of diverse and include camouflage NSW, Australia.
strong antioxidants. Additional via counter-illumination, escape- *E-mail: [email protected]

R314 Current Biology 26, R307–R318, April 25, 2016

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