Photobehaviours guided by simple photoreceptor systems

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Abstract

Light provides a widely abundant energy source and valuable sensory cue in nature. Most animals exposed to light have photoreceptor cells and in addition to eyes, there are many extraocular strategies for light sensing. Here, we review how these simpler forms of detecting light can mediate rapid behavioural responses in animals. Examples of these behaviours include photophobic (light avoidance) or scotophobic (shadow) responses, photokinesis, phototaxis and wavelength discrimination. We review the cells and response mechanisms in these forms of elementary light detection, focusing on aquatic invertebrates with some protist and terrestrial examples to illustrate the general principles. Light cues can be used very efficiently by these simple photosensitive systems to effectively guide animal behaviours without investment in complex and energetically expensive visual structures.

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Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice.

S. Hattar, R. J. Lucas, N Mrosovsky … (2003)

In the mammalian retina, besides the conventional rod-cone system, a melanopsin-associated photoreceptive system exists that conveys photic information for accessory visual functions such as pupillary light reflex and circadian photo-entrainment. On ablation of the melanopsin gene, retinal ganglion cells that normally express melanopsin are no longer intrinsically photosensitive. Furthermore, pupil reflex, light-induced phase delays of the circadian clock and period lengthening of the circadian rhythm in constant light are all partially impaired. Here, we investigated whether additional photoreceptive systems participate in these responses. Using mice lacking rods and cones, we measured the action spectrum for phase-shifting the circadian rhythm of locomotor behaviour. This spectrum matches that for the pupillary light reflex in mice of the same genotype, and that for the intrinsic photosensitivity of the melanopsin-expressing retinal ganglion cells. We have also generated mice lacking melanopsin coupled with disabled rod and cone phototransduction mechanisms. These animals have an intact retina but fail to show any significant pupil reflex, to entrain to light/dark cycles, and to show any masking response to light. Thus, the rod-cone and melanopsin systems together seem to provide all of the photic input for these accessory visual functions.

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Bacterial rhodopsin: evidence for a new type of phototrophy in the sea.

O Béjà, L Aravind, E. V. Koonin … (2000)

Extremely halophilic archaea contain retinal-binding integral membrane proteins called bacteriorhodopsins that function as light-driven proton pumps. So far, bacteriorhodopsins capable of generating a chemiosmotic membrane potential in response to light have been demonstrated only in halophilic archaea. We describe here a type of rhodopsin derived from bacteria that was discovered through genomic analyses of naturally occuring marine bacterioplankton. The bacterial rhodopsin was encoded in the genome of an uncultivated gamma-proteobacterium and shared highest amino acid sequence similarity with archaeal rhodopsins. The protein was functionally expressed in Escherichia coli and bound retinal to form an active, light-driven proton pump. The new rhodopsin exhibited a photochemical reaction cycle with intermediates and kinetics characteristic of archaeal proton-pumping rhodopsins. Our results demonstrate that archaeal-like rhodopsins are broadly distributed among different taxa, including members of the domain Bacteria. Our data also indicate that a previously unsuspected mode of bacterially mediated light-driven energy generation may commonly occur in oceanic surface waters worldwide.

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The cryptochromes: blue light photoreceptors in plants and animals.

Inês Chaves, Richard Pokorny, Martin Byrdin … (2011)

Cryptochromes are flavoprotein photoreceptors first identified in Arabidopsis thaliana, where they play key roles in growth and development. Subsequently identified in prokaryotes, archaea, and many eukaryotes, cryptochromes function in the animal circadian clock and are proposed as magnetoreceptors in migratory birds. Cryptochromes are closely structurally related to photolyases, evolutionarily ancient flavoproteins that catalyze light-dependent DNA repair. Here, we review the structural, photochemical, and molecular properties of cry-DASH, plant, and animal cryptochromes in relation to biological signaling mechanisms and uncover common features that may contribute to better understanding the function of cryptochromes in diverse systems including in man.

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Author and article information

Contributors

Emelie Brodrick:

ORCID: http://orcid.org/0000-0001-7349-1494

E.Brodrick@exeter.ac.uk

Journal

Journal ID (nlm-ta): Anim Cogn

Journal ID (iso-abbrev): Anim Cogn

Title: Animal Cognition

Publisher: Springer Berlin Heidelberg (Berlin/Heidelberg )

ISSN (Print): 1435-9448

ISSN (Electronic): 1435-9456

Publication date (Electronic): 31 August 2023

Publication date PMC-release: 31 August 2023

Publication date (Print): 2023

Volume: 26

Issue: 6

Pages: 1817-1835

Affiliations

[1 ]Living Systems Institute, University of Exeter, ( https://ror.org/03yghzc09) Stocker Road, Exeter, EX4 4QD UK

[2 ]Centre for Organismal Studies, University of Heidelberg, ( https://ror.org/038t36y30) 69120 Heidelberg, Germany

Author information

Emelie Brodrick http://orcid.org/0000-0001-7349-1494

Gáspár Jékely http://orcid.org/0000-0001-8496-9836

Article

Publisher ID: 1818

DOI: 10.1007/s10071-023-01818-6

PMC ID: 10770211

PubMed ID: 37650997

SO-VID: 5589a015-8225-4551-b549-44a70c649483

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 15 May 2023

Date revision received : 29 July 2023

Date accepted : 1 August 2023

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004412, Human Frontier Science Program;

Award ID: HFSP-220180

Award Recipient : Emelie Brodrick Gáspár Jékely

Custom metadata

ScienceOpen disciplines: Animal science & Zoology

Keywords: phototaxis,non-visual photoreception,photokinesis,photophobia,scotophobia

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ScienceOpen disciplines: Animal science & Zoology

Keywords: phototaxis, non-visual photoreception, photokinesis, photophobia, scotophobia

Photobehaviours guided by simple photoreceptor systems

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Abstract

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Most cited references 184

Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice.

Bacterial rhodopsin: evidence for a new type of phototrophy in the sea.

The cryptochromes: blue light photoreceptors in plants and animals.

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