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Seasonal variation in UVA light drives hormonal and behavioural changes in a marine annelid via a ciliary opsin

Nature Ecology & Evolution volume 5, pages 204–218 (2021)Cite this article

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Abstract

The right timing of animal physiology and behaviour ensures the stability of populations and ecosystems. To predict anthropogenic impacts on these timings, more insight is needed into the interplay between environment and molecular timing mechanisms. This is particularly true in marine environments. Using high-resolution, long-term daylight measurements from a habitat of the marine annelid Platynereis dumerilii, we found that temporal changes in ultraviolet A (UVA)/deep violet intensities, more than longer wavelengths, can provide annual time information, which differs from annual changes in the photoperiod. We developed experimental set-ups that resemble natural daylight illumination conditions, and automated, quantifiable behavioural tracking. Experimental reduction of UVA/deep violet light (approximately 370–430 nm) under a long photoperiod (16 h light and 8 h dark) significantly decreased locomotor activities, comparable to the decrease caused by a short photoperiod (8 h light and 16 h dark). In contrast, altering UVA/deep violet light intensities did not cause differences in locomotor levels under a short photoperiod. This modulation of locomotion by UVA/deep violet light under a long photoperiod requires c-opsin1, a UVA/deep violet sensor employing Gi signalling. C-opsin1 also regulates the levels of rate-limiting enzymes for monogenic amine synthesis and of several neurohormones, including pigment-dispersing factor, vasotocin (vasopressin/oxytocin) and neuropeptide Y. Our analyses indicate a complex inteplay between UVA/deep violet light intensities and photoperiod as indicators of annual time.

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Fig. 1: Light intensity ratios provide seasonal information that is different from that provided by the photoperiod.
Fig. 2: UVA/deep violet light affects locomotor behaviour in P. dumerilii.
Fig. 3: P. dumerilii c-opsin1 mediates UVA/deep violet light input via Gi signalling and regulates locomotor activity.
Fig. 4: Loss of c-opsin1 affects brain hormone synthesis.

Data availability

All of the data generated or analysed during this study are included within the published article and its Supplementary Information files. The targeted mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium (http://proteomecentral.proteomexchange.org) via Panorama Public99 with the identifier PXD014682. The light and temperature measurements and untargeted proteomics raw data have been deposited at Dryad (https://doi.org/10.5061/dryad.73n5tb2vv).

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Acknowledgements

We thank the members of the Tessmar-Raible and Raible groups for discussions; A. Belokurov and M. Borysova for excellent worm care at the MFPL aquatic facility; M. Waldherr, L. Orel and N. Getachew for excellent technical assistance; and N. Hartl for technical assistance with the PRM assays. Targeted proteomics experiments were performed using the Vienna BioCenter Core Facilities (VBCF) instrument pool. K.T.-R. received funding for this research from: the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007–2013; ERC grant agreement 337011) and the Horizon 2020 Programme (ERC grant agreement 819952); the research platform ‘Rhythms of Life’ of the University of Vienna; the Austrian Science Fund (FWF; http://www.fwf.ac.at/en/), including a START award (AY0041321), research project grant (P28970) and SFB grant (SFB F78); and the HFSP (http://www.hfsp.org/; research grant RGY0082/2010). None of the funding bodies were involved in the design of the study, the collection, analysis and interpretation of data, or in writing the manuscript.

Author information

Author notes

  1. Enrique Arboleda

    Present address: Institut de Génomique Fonctionnelle de Lyon (IGFL), École Normale Supérieure de Lyon, Lyon, France

  2. Maximillian Hofbauer

    Present address: loopbio, Vienna, Austria

Authors and Affiliations

  1. Max Perutz Labs, Vienna BioCenter, University of Vienna, Vienna, Austria

    Vinoth Babu Veedin Rajan, N. Sören Häfker, Enrique Arboleda, Birgit Poehn, Thomas Gossenreiter, Maximillian Hofbauer, Markus Hartl & Kristin Tessmar-Raible

  2. Research Platform ‘Rhythms of Life’, Vienna BioCenter, University of Vienna, Vienna, Austria

    Vinoth Babu Veedin Rajan, N. Sören Häfker, Enrique Arboleda, Birgit Poehn, Maximillian Hofbauer & Kristin Tessmar-Raible

  3. Division of Neuroscience and Experimental Psychology, University of Manchester, Manchester, UK

    Elliot Gerrard & Robert J. Lucas

  4. Marine Breeding Systems, St. Gallen, Switzerland

    Christian Mühlestein

  5. Department of Analytical Chemistry, Faculty of Chemistry, University of Vienna, Vienna, Austria

    Andrea Bileck & Christopher Gerner

  6. Stazione Zoologica Anton Dohrn, Napoli, Italy

    Maurizio Ribera d’Alcala & Maria C. Buia

Authors
  1. Vinoth Babu Veedin Rajan
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  2. N. Sören Häfker
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  3. Enrique Arboleda
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  4. Birgit Poehn
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  5. Thomas Gossenreiter
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  6. Elliot Gerrard
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  7. Maximillian Hofbauer
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  8. Christian Mühlestein
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  9. Andrea Bileck
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  10. Christopher Gerner
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  11. Maurizio Ribera d’Alcala
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  12. Maria C. Buia
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  13. Markus Hartl
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  14. Robert J. Lucas
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  15. Kristin Tessmar-Raible
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Contributions

V.B.V.R. conducted the experimental work, planned parts of the project, analysed and interpreted the data and designed the figures and data representation for the entire manuscript with additional contributions by others outlined as follows. N.S.H. performed data analyses and interpretation, figure design of the untargeted proteomics experiments, and provided detailed input to writing the ecological parts of the manuscript. E.A. performed the natural light and temperature measurements and data analyses. B.P. conducted the indoor light measurements and helped to design the automated worm locomotor analysis set-up and NELIS. T.G. and M.H. acquired and analysed the targeted proteomics data. E.G. and R.J.L. helped to perform the experimental work and data analyses, designed the experimental plans for the c-Opsin action spectrum and signalling and helped to calculate the Opsin R/M state ratios. M.H. designed the automated worm locomotor analysis set-up. C.M. designed the NELIS illumination set-ups. A.B. and C.G. performed the untargeted proteomics data acquisition and analyses. M.R.d’A. helped to perform the natural light and temperature measurements and provided detailed feedback on ecological perspectives. M.C.B helped to perform the natural light and temperature measurements. K.T.-R. planned the project, conceived of the experimental concepts, discussed, analysed and interpreted the data and wrote the manuscript. All authors provided comments and feedback to the manuscript.

Corresponding author

Correspondence to Kristin Tessmar-Raible.

Ethics declarations

Competing interests

M.H. is the chief executive officer of loopbio, a company developing commercial animal behavioural tracking solutions. C.M. is the chief executive officer of Marine Breeding Systems, a company developing commercial illumination systems for aquaculture. All other authors declare no competing interests.

Additional information

Peer review information Nature Ecology and Evolution thanks Oren Levy and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Benchmarking of daylight intensity measurements at 10 m with published measurements and calculations.

The units from our data are in each case converted and plotted corresponding to the units and type of plot used in the respective compared publication. (a) Nightlight data measured for individual wavelengths between August 24–25, 1999100. (b,c) Analysis from (a) performed on natural light data measurement for August 24–25 2010. (c): saturation and noise-equivalent irradiance thresholds are indicated 400 nm (pink line), 500 nm (green line) and 700 nm (red line). (d) Calculations of light irradiance at different ocean depths101. Black arrow points at UVA spectral range clearly present at 10 m water depth and below. (e,f) Our measurements from July 4, 2011 and August 24, 2010 at 12:00 noon for comparison. (g) Irradiance data calculated for different water depths based on in situ measurements of the attenuation coefficients in coastal waters in Corsica using a PhotoreSearch PR-670 spectrophotometer in a custom UW housing on July 4th, 2010, under bright sun at noon102. (h,i) Our measurements from July 4, 2011 at 12:00 noon timepoint. (j) Irradiance in atmosphere and in water at different depths103. (k,l) Representative daylight measurements from July 4, 2011 and August 24, 2010 at 12:00 noon timepoint from our 10 m measurement set for comparsion. (m,n) Average spectral irradiance and individual wavelength penetration under different ocean depths104. (f,i,l) Examplary saturation and noise equivalent irradiance (NEI) levels of the RAMSES hyperspectral radiometer indicated as dots. Panel a reproduced with permission from ref. 100, Springer Nature Ltd; d reproduced with permission from ref. 101, Cambridge University Press; g reproduced with permission from ref. 102, Elsevier; j reproduced with permission from ref. 66, Mary Ann Liebert, Inc.; m and n reproduced with permission from ref. 104, Oxford University Press.

Extended Data Fig. 2 Daytime spectral irradiance and ratios with and without twilight (10 m depth).

(a) Daylight average per day across the year between sunrise to sunset without twilight times for each wavelength. For 3D-rotational graph: Supplementary Data 2. (b) 2-D pcolor plot of (a). (c) Daylight spectrum across the year for each wavelength between astronomical dawn to astronomical dusk (raw data). For 3D-rotational graph: Supplementary Data 3. (d) 2-D pcolor plot of (c). (e) Daytime monthly irradiance averages comparing periods of equal photoperiods. Long day photoperiod example: 14 April – 15 May 2011 (yellow) and 27 July – 27 August 2010 (blue), short day photoperiod example: 9 January – 9 February 2011 (black) and 1 November – 2 December 2010 (red). (f, g) Equinox day spectra without twilight (f) and between astronomical twilight (g). For 3D-plot: Supplementary Data 6 and 9. (h,i) Screenshot of weather data for spring and autumnal equinox days: https://www.timeanddate.com/weather. (j, k) 3D-surface plot of equinox day ratio - September 23, 2010/March 21, 2011 (j) and September 23, 2010/March 24, 2011 (k). For 3D-rotational graph: Supplementary Data 7 and 8. (l) Ratios of wavelengths averaged across the day for fall and spring equinox days including twilight times. Black dotted lines: range of strong c-opsin1 activation. Data were corrected for daylight saving time.

Extended Data Fig. 3 Irradiance differences between 4 m and 10 m water depth.

(a,b) Daylight spectra without twilight of 4 m (a) and 10 m (b) water depth during June 2011. For 3D-rotational graph: Supplementary data 4 and 5. (c,d) Monthly average 2D plot of (a,b) in logarithmic (c) and in linear scale (d). Blue: 4 m, Red: 10 m. (e) Wavelength ratios between monthly average of June 2011-4 m/June 2011-10 m. (f,g) Zoom-in for specific wavelengths ranges from plot (d) for better visualization. Black dotted lines: range of strong c-opsin1 activation. Data were corrected for daylight saving time shifts.

Extended Data Fig. 4 Light spectra and intensity data for experimental light sources.

(a-e) Light intensity and spectra measured using an ILT950 spectrometer (International Light Technologies Inc, Peabody, USA) for (a) standard worm culture illumination, (b,b’) worm culture using ‘NELIS’ in linear plot (b) and logarithmic plot (b’), (c,c’) Behavioural chamber with ‘Nelis’ white light with UVA as linear plot (c) and logarithmic plot (c’). (d,d’) Behavioural chamber with ‘Nelis’ white light and a filter reducing light below 430 nm (UVAR filter, Pixelteq, Salvo Technologies, USA) as linear plot (d) and logarithmic plot (d’), (e,e’) Behavioural chamber with ‘Nelis’ white light matching the intensities of the spectrum >430 nm from (d,d’) as linear (e) and logarithmic plot (e’). Purple dotted line in b-e indicates the c-opsin1 high activation range. (f,g) Picture details of ‘Nelis’ light source.

Extended Data Fig. 5 G-protein signaling analyses, irradiance dose response curves and spectral sensitivity analyses of Platynereis c-opsin1.

(a) Broad spectrum white light from Arc lamp used for G-protein selectivity assay. (b) Wavelength spectra from CoolLED light source used for spectral characterization of Platynereis c-opsin1. (c) Cells transfected with Platynereis c-opsin1 showed no increase in calcium concentration after 2 s white light pulse in calcium bioluminescence assay testing for G𝛼q binding (purple diamonds: Pdu-c-opsin1, red open circles: human melanopsin, black inverted triangles: no opsin, black arrow: 2 s white light pulse). (d) No luminescence increase after 30 s white light pulse indicates that Platynereis c-opsin1 does not signal via G𝛼s (Pdu c-opsin1, Purple diamond; Jellyopsin, red open triangle; no opsin, black inverted triangle; 30 s white light pulse, black arrow). (e) Schematic diagram of Platynereis c-opsin1 chimera with second and third intracellular loop regions replaced by corresponding human melanopsin loop region and downstream signaling. (f) Platynereis c-opsin1-human melanopsin chimera depicted in (e) shows a clear response in the calcium luminescence assay, indicative of G𝛼q-signaling. (g-m) Irradiance dose response curve of Platynereis c-opsin1-melanopsin chimera at 7 different wavelengths.

Extended Data Fig. 6 Platynereis c-opsin1Δ8/Δ8 allele exhibit lowered locomotor activity under longday, including UVA during LD and DD.

(a-c) Double plotted average actogram plot of c-opsin1+/+ (a: n = 17), c-opsin1Δ8/+ (b: n = 12) and c-opsin1Δ8/Δ8 worms (c: n = 20) under longday, including strong UVA under Light-Dark (LD, days 1-5) and Dark-Dark condition (DD, days 6-10, grey shaded). (d) Significant difference in rhythmicity power (PN) exist for c-opsin1Δ8/+ vs c-opsin1Δ8/Δ8 and c-opsin1+/+ vs c-opsin1Δ8/Δ8, but not for c-opsin1+/+ vs c-opsin1Δ8/+ (Mann-Whitney-Wilcoxon test). (e) Percentage of rhythmicity calculated for all genotypes under LD condition (c-opsin1+/+: 100%R, c-opsin1Δ8/+: 100%R and c-opsin1Δ8/Δ8: 90%R+10%WR). (f) c-opsin1Δ8/Δ8 worms showed significant decrease in nocturnal locomotor activity compared to c-opsin1+/+ and c-opsin1Δ8/+ (One-way ANOVA with Sidak’s multiple comparison test). (g) Under DD free-running conditions, significant differences in rhythmicity power (PN) exist for c-opsin1+/+ vs c-opsin1Δ8/Δ8 and c-opsin1+/+ vs c-opsin1Δ8/+, but no difference for c-opsin1Δ8/+ vs c-opsin1Δ8/Δ8 (Mann-Whitney-Wilcoxon test). (h) Percentage of rhythmicity calculated for all genotypes under DD condition (c-opsin1+/+: 76.48%R+17.64%WR+5.88%AR, c-opsin1Δ8/+: 33.33%R+41.67%WR+25%AR and c-opsin1Δ8/Δ8: 30%R+30%WR+40%AR). (i) c-opsin1Δ8/Δ8 worms recorded under DD condition showed significant decrease in nocturnal locomotor activity compared to c-opsin1+/+ and c-opsin1Δ8/+ (One-way ANOVA with Sidak’s multiple comparison test). *p<0.05, ** p<0.01, *** p<0.001. For individual actograms see Supplementary Fig. 2.

Extended Data Fig. 7 Platynereis c-opsin1Δ8/Δ7 transheterozygous worms exhibit lowered locomotor activity under longday, including UVA conditions.

(a,b) Average, double-plotted actogram of c-opsin1+/+ (a: n = 15), c-opsin1Δ8/Δ7 (b: n = 21). 3 days of LD. (c) No difference in power (PN) was observed between c-opsin1+/+ and c-opsin1Δ8/Δ7 (Mann-Whitney-Wilcoxon test). (d) Percentage of rhythmicity calculated for all genotypes under LD condition (c-opsin1+/+: 80%R+13.33WR+6.67AR; c-opsin1Δ8/Δ7: 57.14%R+14.29%WR+28.57AR). (e) c-opsin1Δ8/Δ7 worms showed a significant decrease in nocturnal locomotor activity compared to c-opsin1+/+ (One-way ANOVA with sidak’s multiple comparison test). *p<0.05, ** p<0.01, *** p<0.001. For individual actograms see Supplementary Fig. 3.

Extended Data Fig. 8 Locomotion under long day (LD 16:8) and intermediate photoperiod (LD 12:12) with full and filter-reduced UVA.

Locomotor behaviour of Platynereis c-opsin1Δ8/Δ8 mutant and its corresponding wt siblings. (a,b) Double plotted average actograms of c-opsin1+/+ worms under long day Nelis white light with intense UVA (+UVA) (a: n = 12) and with filter-reduced UVA (-UVA) (b: n = 10). (c) c-opsin1+/+ worms under –UVA conditions showed a significantly decrease locomotor activity compared to worms under +UVA conditions and (d) significant decrease in power (PN) and rhythmicity. (e,f) Double plotted average actograms of c-opsin1Δ8/Δ8 worms under LD16:8 +UVA (e, n = 11) and -UVA (f, n = 10). (g,h) c-opsin1Δ8/Δ8 worms recorded in (e,f) showed no difference in locomotor activity level (g) and rhythmicity (h). (i,j) Double plotted average actograms of c-opsin1+/+ worms under LD 12:12 +UVA (i: n = 9) and -UVA (j: n = 7). (k,l) c-opsin1+/+ worms recorded in (i,j) with a difference in locomotor activity close to statistical significance (k), and no difference in rhythmicity (l). (m,n) Double plotted average actograms of c-opsin1Δ8/Δ8 worms under LD 12:12 +UVA (m: n = 10) and -UVA (n: n = 9). (o,p) c-opsin1Δ8/Δ8 worms recorded in (m,n) showed no difference trend in locomotor activity level (o) and rhythmicity (p). For all statistical comparisons and p values: Supplementary Fig. 7. Statistics: locomotor activity: One-way ANOVA, Sidak’s multiple comparison test, period, power and rhythmicity: Individual worm rhythmicity and power were determined via Lomb-Scargle periodograms using ActogramJ. The averages of multiple worms were tested by Mann-Whitney-Wilcoxon test. *p<0.05, ** p<0.01, *** p<0.001. Locomotor data of individual worms: Supplementary Figs. 8, 9.

Extended Data Fig. 9 Head transcript level analyses for additional candidate genes in c-opsin1Δ/8Δ8 and corresponding wildtypes.

Genes as indicated in each panel. The p-value for differences across time was determined by one-way ANOVA. One-way ANOVA with Sidak’s multiple comparison test was used for differences at specific timepoints. Differences between overall transcript levels (measured as AUC) were tested for by Unpaired student’s t-test with Welch’s correction. n.s.- non significant Data displayed as mean± S.E.M., n = 3BR (5 heads/BR).

Extended Data Fig. 10 Overview of untargeted proteomics experiment under UVA condition.

(a) UVA light used for untargeted proteomics experiment on c-opsin1+/+ and c-opsin1Δ8/Δ8 worms. (b) Sampling scheme. (c) Cellular and pathway model representing differentially regulated protein candidates. For primary data see: Supplementary Tables 13–15. N = 3BRs (20heads/BR), The significance was calculated by two-sided students t-test with adjusted p-value 0.05 (Permutation based FDR correction). Only proteins with least 2 peptides (at least one of it unique) were included in analyses.

Supplementary information

Supplementary Information

Supplementary Figs. 1–10.

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Supplementary Data 1

Rotatable 3D plot corresponding to the stationary image in Fig. 1c.

Supplementary Data 2

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 2a.

Supplementary Data 3

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 2c.

Supplementary Data 4

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 3a.

Supplementary Data 5

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 3b.

Supplementary Data 6

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 2f.

Supplementary Data 7

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 2j.

Supplementary Data 8

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 2k.

Supplementary Data 9

Rotatable 3D plot corresponding to the stationary image in Extended Data Fig. 2g.

Supplementary Tables

Supplementary Tables 1–17. Primary data from measurements, as well as calculations and statistics (for details, see the individual tab labels).

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Veedin Rajan, V.B., Häfker, N.S., Arboleda, E. et al. Seasonal variation in UVA light drives hormonal and behavioural changes in a marine annelid via a ciliary opsin. Nat Ecol Evol 5, 204–218 (2021). https://doi.org/10.1038/s41559-020-01356-1

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