Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

Revilla-i-Domingo, Roger; Rajan, Vinoth Babu Veedin; Waldherr, Monika; Prohaczka, Günther; Musset, Hugo; Orel, Lukas; Gerrard, Elliot; Smolka, Moritz; Stockinger, Alexander; Farlik, Matthias; Lucas, Robert J.; Raible, Florian; Tessmar-Raible, Kristin

doi:10.7554/elife.66144

Cited by 13 publications

(4 citation statements)

References 99 publications

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“…This illustrates that activity was present and the comparison with worms that crawled out of the tracking well ( S7B and S7C Fig ) confirms that this is not “background noise,” but actual worm movement. The reoccurring activity spikes visible in the magnification can further be attributed to normal worm behavior (moving/turning in tube, respiratory undulations) [ 37 , 83 ], and activity of arrhythmic worms in general is highly similar to that of rhythmic worms during (subjective) daytime in both LD and DD ( S6 Fig ). Additionally, as some worms matured between the behavioral characterization and the sampling for RNAseq (see below), we could see that rhythmic and arrhythmic worms did this in exactly the same way and with the same reproductive success.…”

Section: Methodsmentioning

confidence: 99%

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Häfker,

Holcik,

Mat

et al. 2024

PLoS Biol

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The circadian clock controls behavior and metabolism in various organisms. However, the exact timing and strength of rhythmic phenotypes can vary significantly between individuals of the same species. This is highly relevant for rhythmically complex marine environments where organismal rhythmic diversity likely permits the occupation of different microenvironments. When investigating circadian locomotor behavior of Platynereis dumerilii, a model system for marine molecular chronobiology, we found strain-specific, high variability between individual worms. The individual patterns were maintained for several weeks. A diel head transcriptome comparison of behaviorally rhythmic versus arrhythmic wild-type worms showed that 24-h cycling of core circadian clock transcripts is identical between both behavioral phenotypes. While behaviorally arrhythmic worms showed a similar total number of cycling transcripts compared to their behaviorally rhythmic counterparts, the annotation categories of their transcripts, however, differed substantially. Consistent with their locomotor phenotype, behaviorally rhythmic worms exhibit an enrichment of cycling transcripts related to neuronal/behavioral processes. In contrast, behaviorally arrhythmic worms showed significantly increased diel cycling for metabolism- and physiology-related transcripts. The prominent role of the neuropeptide pigment-dispersing factor (PDF) in Drosophila circadian behavior prompted us to test for a possible functional involvement of Platynereis pdf. Differing from its role in Drosophila, loss of pdf impacts overall activity levels but shows only indirect effects on rhythmicity. Our results show that individuals arrhythmic in a given process can show increased rhythmicity in others. Across the Platynereis population, rhythmic phenotypes exist as a continuum, with no distinct “boundaries” between rhythmicity and arrhythmicity. We suggest that such diel rhythm breadth is an important biodiversity resource enabling the species to quickly adapt to heterogeneous or changing marine environments. In times of massive sequencing, our work also emphasizes the importance of time series and functional tests.

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Section: Methodsmentioning

confidence: 99%

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Häfker,

Holcik,

Mat

et al. 2024

PLoS Biol

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“…This mechanosensory modulation function does not require a retinal-based chromophore ( 125 ). This might represent a loss of an originally existing light-depending mechanosensory modulation, as in the bristle worm Platynereis dumerilii , an orthologous opsin functions in a light-dependent manner in likely mechanosensory cells to modulate the worms’ undulatory “breathing” movements ( 126 ). It is also noteworthy that the cellular signaling of these kinds of rhabdomeric opsins typically involves membrane stretch, which could provide a possible mechanistic explanation for its role in the bristle worm ( 126 ).…”

Section: Functions Other Than Light Perception?mentioning

confidence: 99%

All Light, Everywhere? Photoreceptors at Nonconventional Sites

Mat,

Vu,

Wolf

et al. 2024

Physiology

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One of the biggest environmental alterations we have made to our species is the change in the exposure to light. During the day we typically sit behind glass windows illuminated by artificial light that is >400 times dimmer and has a very different spectrum than natural daylight. On the opposite end are the nights that are now lit up by several orders of magnitude. This review aims to provide food for thought as to why this matters for humans and other animals. Evidence from behavioral neuroscience, physiology, chronobiology and molecular biology is increasingly converging on the conclusions that the biological non-visual functions of light and photosensory molecules are highly complex. The initial work of von Frisch on extraocular photoreceptors in fish, the identification of rhodopsins as the molecular light receptors in animal eyes and eye-like structures and cryptochromes as light sensors in non-mammalian chronobiology still allowed for the impression that light reception would be a relatively restricted, localized sense in most animals. However, light-sensitive processes and/or sensory proteins have now been localized to many different cell types and tissues. It might be necessary to consider non-light responding cells as the exception, rather than the rule.

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“…In addition, we recovered multiple semaphorin transcripts involved in axon guidance (SEMA5B) (81), transducins GNAT1 and GNAT2 (82), and opsin of the cnidops family (14,15). Adhesion GPCR V1 (ADGRV1), associated with nervous system development (83), and myosin III (MYO3B, MYO3A) an actin-based motor protein with kinase activity present in photoreceptors and stereocilia in general, are also differentially expressed (84)(85)(86). The involvement of structural and physiological loci in the development of phototactic planulae suggests that many of these components were present in ciliated photosensory, or multisensory neurons in the ancestor of cnidarians and bilaterians (23,87).…”

Section: Developmental Transcriptomics Implicate Photosensation and S...mentioning

confidence: 99%

Phototactic preference and its genetic basis in the planulae of the colonial Hydrozoan Hydractinia symbiolongicarpus

Birch,

McGee,

Provencher

et al. 2024

Preprint

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Background Marine organisms with sessile adults commonly possess motile larval stages that make settlement decisions based on integrating environmental sensory cues. Phototaxis, the movement toward or away from light, is a common behavioral characteristic of aquatic and marine metazoan larvae, as well as of algae, protists, and fungi. In cnidarians, behavioral genomic investigations of motile planulae larvae have been conducted in anthozoans (corals and sea anemones) and scyphozoans (true jellyfish), but such studies are presently lacking in hydrozoans. Here, we examined the behavioral genomics of phototaxis in planulae of the hydrozoan Hydractinia symbiolongicarpus. Results A behavioral phototaxis study of day 3 planulae indicated preferential phototaxis to green (523 nm) and blue (470 nm) wavelengths of light, but not red (625 nm) wavelengths. A developmental transcriptome study where planula larvae were collected from four developmental time points for RNA-seq revealed that many genes critical to the physiology and development of ciliary photosensory systems are dynamically expressed in planula development and correspond to the expression of phototactic behavior. Microscopical investigations using immunohistochemistry and in situ hybridization demonstrated that several transcripts with predicted function in photoreceptors, including cnidops class opsin, CNG ion channel, and CRX-like transcription factor, localize to ciliated bipolar sensory neurons of the aboral sensory neural plexus, which is associated with the direction of phototaxis and the site of settlement. Conclusions The phototactic preference displayed by planulae is consistent with the shallow sandy marine habitats they experience in nature. Our genomic investigations add further evidence of similarities between cnidops-mediated photoreceptors of hydrozoans and other cnidarians and ciliary photoreceptors as found in the eyes of humans and other bilaterians, suggesting aspects of their shared evolutionary history.

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Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

Cited by 13 publications

References 99 publications

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

All Light, Everywhere? Photoreceptors at Nonconventional Sites

Phototactic preference and its genetic basis in the planulae of the colonial Hydrozoan Hydractinia symbiolongicarpus

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