Dawn of Molecular Biology of Infrared Vision

Contributed by: Shozo Yokoyama

Humans visualize a narrow range, 400-700 nanometer (nm), of electromagnetic radiation (light), which is reflected from the surfaces of various objects in nature.  In addition to the photochemical detection of light, certain animals and insects have acquired infrared (IR) vision during evolution.  IR is electromagnetic radiation with longer wavelength (750 nm - 1 mm) than those of the visible light.  Much of the energy we receive from the sun is IR radiation, but the IR radiation also includes the thermal radiation emitted by animals.  Organisms with IR vision detect the thermal radiation (750-1,200 nm) for hunting and thermoregulation. 

Fig. 1. Pit viper pit organ.

Only four vertebrates (pit vipers, boas, pythons, and vampire bats) are known to detect and localize sources of infrared (IR) radiation.  Their infrared “eyes” can be one pair (pit vipers and vampire bats) or as many as 13 pairs (boas and pythons) of deep cavities located beneath their eyes, called pit organs (Fig. 1).  In the rattlesnake, the pit organs contain an inner chamber that is separated by a thin (15 mm), concave IR-sensitive membrane (Fig. 2) (1).  The IR and visible-light information are integrated in the brain to yield a unique wide-spectrum picture of the world (2).  Since the postulation that such pit organs can be capable of detecting subtle environmental stimuli (3), the anatomy of the pit organs and the behavioural consequences of IR vision have been extensively studied.  Having no IR receptors in hand, however, little is known about the molecular basis of IR vision.  Thanks to the discovery of the IR receptors by David Julius and his colleagues at UCSF (4, 5), this 80-year stalemate is going to be overcome.  Before these papers were published, it had been suspected that IR receptors operate on a thermal principle rather than photochemical principle (e.g. (6)), suggesting that the transient receptor potential (TRP) ion channels may be involved.

      Fig. 2. Rattlesnake pit organ, (1).                  

 

The TRP ion channels are involved in a diverse range of biological processes, including calcium and magnesium homeostasis, neuronal growth, temperature sensation, and pain sensation (7, 8).  Based on sequence similarity, the TRP superfamily can be divided into seven subfamilies: TRPC (canonical), TRPV (vanilloid), TRPM (melastatin), TRPA (ankyrin), TRPN (NOMPC), TRPP (polycystin), and TRPML (mucolipin) (Fig. 3).  The total numbers of TRP channels in worm (C. elegans), fruit fly (D. melanogaster), mouse (M. musculus), and human vary between 13 and 28 (8).  So, which TRP receptor is involved in the IR vision? 

Fig. 3. Some examples of TRP receptors, (8).

The best candidates for the IR receptors are TRPVs because of their sensitivities to body-heat and external temperatures.  For example, TRPV1, 2, 3, and 4 are activated at 43, 52, 39, and 27-34 ^oC, respectively.  However, in the first paper (4), Gracheva et al. have shown that the IR receptors isolated from the western diamondback rattlesnake (Crotalus atrox), ball python (Python regius), and garden tree boa (Corallus hortulanus) are TRPA1s.  Many people may have personally experienced the fiery sensation caused by wasabi when eating sushi.  This sensation is initiated by our TRPA1 receptors.  The paper contains an enormous amount of data on the molecular cloning and expression of TRPA1s, omics, and some molecular evolution not only of the three evolutionarily distantly related rattlesnake, python, and boa but also of the Texas rat snake (Pantherophis obsoletus lindheimeri) without IR vision.  Interestingly, the rattlesnake is evolutionarily more closely related to the rat snake than to the python or the boa, suggesting the independent origin of IR vision among the snakes.

Knowing that the snakes use TRPA1 for their IR vision, we might now think that vampire bats (Desmodus rotundus) also modified TRPA1 to detect IR.  We are wrong again!  The second and equally wonderful paper (5) reveals that the vampire bat after all uses one of the TRPVs, TRPV1, for its IR vision.  One fascinating feature is that the bat IR-detection has been achieved through alternative splicing of the TRPV1 transcript that produces a truncated receptor, which is caused by a newly acquired extra exon of 29 nucleotides.

The discoveries of the IR receptors in the snakes and vampire bat will open an exciting new chapter in the molecular analyses of signal transduction underlying IR detection.  Molecular evolutionary studies of the two sets of IR-sensitive and other TRP receptors will be helpful not only in understanding the mechanisms of IR vision but also in elucidating the mechanisms of phenotypic differentiation of diverse TRP superfamily members. 

References

1.  E. A. Newman, P. H. Hartline, The infrared 'vision' of snakes. Sci. Amer. 20, 116 (1982).

2.  E. A. Newman, P. H. Hartline, Integration of visual and infrared information in bimodal neurons in the rattlesnake optic tectum. Science 213, 789 (Aug 14, 1981).

3.  W. G. Lynn, The structure and function of the facial pit of the pit vipers. American Journal of Anatomy 49, 97 (1931).

4.  E. O. Gracheva et al., Molecular basis of infrared detection by snakes. Nature 464, 1006 (Apr 15, 2010).

5.  E. O. Gracheva et al., Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 476, 88 (Aug 4, 2011).

6.  J. F. Harris, R. I. Gamow, Snake infrared receptors: thermal or photochemical mechanism? Science 172, 1252 (Jun 18, 1971).

7.  R. Gaudet, A primer on ankyrin repeat function in TRP channels and beyond. Mol Biosyst 4, 372 (May, 2008).

8.  K. Venkatachalam, C. Montell, TRP channels. Annu Rev Biochem 76, 387 (2007).