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Many marine animals, ranging from corals to fishes, synchronise reproduction to lunar cycles. In the annelid Platynereis dumerilii, this timing is orchestrated by an endogenous monthly (circalunar) clock entrained by moonlight. Whereas daily (circadian) clocks cause extensive transcriptomic and proteomic changes, the quality and quantity of regulations by circalunar clocks have remained largely elusive. By establishing a combined transcriptomic and proteomic profiling approach, we provide first systematic insight into the molecular changes in Platynereis heads between circalunar phases, and across sexual differentiation and maturation. Whereas maturation elicits large transcriptomic and proteomic changes, the circalunar clock exhibits only minor transcriptomic, but strong proteomic regulation. Our study provides a versatile extraction technique and comprehensive resources. It corroborates that circadian and circalunar clock effects are likely distinct and identifies key molecular brain signatures for reproduction, sex and circalunar clock phase. Examples include prepro-whitnin/proctolin and ependymin-related proteins as circalunar clock targets. Like many other sea creatures, the worm Platynereis dumerilii reproduces by dispersing eggs and sperm in the water. For these animals, timing is everything: if they fail coordinate their release, the precious reproductive cells will drift in the vastness of the ocean without ever meeting their male or female counterparts. Internal clocks are a set of mechanisms that allow organisms to tune their internal processes to their environment. For example, the circadian clock helps many creatures to adapt to the cycle of day and night. This involves switching genes on and off according to the time of day. When a gene is activated, its information is copied into a molecule of RNA, which is then read to create proteins that will go on performing specific roles. To produce their eggs and sperm at the right time, P. dumerilii worms rely on a poorly understood internal clock which is synchronized by the moon cycle. To investigate this ‘inner calendar’, Schenk, Bannister et al. developed a new technique that allows them to extract both RNA and proteins from the miniscule heads of the worms. The results showed that the internal clock synchronized by the lunar phases influenced the levels of many more proteins than RNA molecules. In comparison, other life events such as the worms becoming sexually mature, had a more similar impact on both protein and RNA regulation. This might suggest that the inner calendar that coordinates the worms with the moon cycle could work by changing protein, rather than RNA levels. The analysis also highlighted several molecular actors that may be essential for the worm’s inner clock to work properly. In the future, the new technique will help to dissect more finely how P. dumerilii and many other marine creatures stay synchronized with the moon, and spawn at the right time.

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor-cell evolution in animals. The two cell types coexist in some animals, however how these cells functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming in non-directional UV light, a behavior absent in ciliary-opsin knockout larvae. UV avoidance overrides positive phototaxis mediated by the rhabdomeric eyes such that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during vertical migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptor cells in a zooplankton larva. The animal kingdom contains many different types of eyes, but all share certain features in common. All detect light using specialized cells called photoreceptors, of which there are two main kinds: ciliary and rhabdomeric. Crustaceans and their relatives, including insects, have rhabdomeric photoreceptors; while animals with backbones, including humans, have ciliary photoreceptors. There are also several groups of animals, mostly sea-dwellers, that inherited both types of photoreceptors from their ancestors that lived millions of years ago. These include the marine ragworm, Platynereis dumerilii. The larvae of Platynereis are free-swimming plankton. Each has a transparent brain and six small, pigmented eyes. The eyes contain rhabdomeric photoreceptors. These enable the larvae to detect and swim towards light sources. Yet the larval brain also contains ciliary photoreceptors, the role of which was unknown. Verasztó, Gühmann et al. now show that ultraviolet light activates ciliary photoreceptors, whereas cyan, or blue-green, light inhibits them. Shining ultraviolet light onto Platynereis larvae makes the larvae swim downwards. By contrast, cyan light makes the larvae swim upwards. In the ocean, ultraviolet light is most intense near the surface, while cyan light reaches greater depths. Ciliary photoreceptors thus help Platynereis to avoid harmful ultraviolet radiation near the surface. Though if the larvae swim too deep, cyan light inhibits the ciliary photoreceptors and activates the rhabdomeric pigmented eyes. This makes the larvae swim upwards again. Using high-powered microscopy, Verasztó, Gühmann et al. confirm that neural circuits containing ciliary photoreceptors exchange messages with circuits containing rhabdomeric photoreceptors. This suggests that the two work together to form a depth gauge. By enabling the larvae to swim at a preferred depth, the depth gauge influences where the worms end up as adults. Its discovery should also stimulate new ideas about the evolution of eyes and photoreceptors.

Rhabdomeric opsins (r-opsins) are light sensors in cephalic eye photoreceptors, but also function in additional sensory organs. This has prompted questions on the evolutionary relationship of these cell types, and if ancient r-opsins were non-photosensory. A molecular profiling approach in the marine bristleworm Platynereis dumerilii revealed shared and distinct features of cephalic and non-cephalic r-opsin1 -expressing cells. Non-cephalic cells possess a full set of phototransduction components, but also a mechanosensory signature. Prompted by the latter, we investigated Platynereis putative mechanotransducer and found that nompc and pkd2.1 co-expressed with r-opsin1 in TRE cells by HCR RNA-FISH. To further assess the role of r-Opsin1 in these cells, we studied its signaling properties and unraveled that r-Opsin1 is a Gαq-coupled blue light receptor. Profiling of cells from r-opsin1 mutants versus wild-types, and a comparison under different light conditions reveals that in the non-cephalic cells light – mediated by r-Opsin1 – adjusts the expression level of a calcium transporter relevant for auditory mechanosensation in vertebrates. We establish a deep-learning-based quantitative behavioral analysis for animal trunk movements and identify a light– and r-Opsin-1–dependent fine-tuning of the worm's undulatory movements in headless trunks, which are known to require mechanosensory feedback. Our results provide new data on peripheral cell types of likely light sensory/mechanosensory nature. These results point towards a concept in which such a multisensory cell type evolved to allow for fine-tuning of mechanosensation by light. This implies that light-independent mechanosensory roles of r-opsins may have evolved secondarily.

The moon’s monthly cycle synchronizes reproduction in countless marine organisms. The mass-spawning bristle worm Platynereis dumerilii uses an endogenous monthly oscillator set by full moon to phase reproduction to specific days. But how do organisms recognize specific moon phases? We uncover that the light receptor L-Cryptochrome (L-Cry) discriminates between different moonlight durations, as well as between sun- and moonlight. A biochemical characterization of purified L-Cry protein, exposed to naturalistic sun- or moonlight, reveals the formation of distinct sun- and moonlight states characterized by different photoreduction- and recovery kinetics of L-Cry’s co-factor Flavin Adenine Dinucleotide. In Platynereis , L-Cry’s sun- versus moonlight states correlate with distinct subcellular localizations, indicating different signaling. In contrast, r-Opsin1, the most abundant ocular opsin, is not required for monthly oscillator entrainment. Our work reveals a photo-ecological concept for natural light interpretation involving a “valence interpreter” that provides entraining photoreceptor(s) with light source and moon phase information. Reproduction in numerous marine organisms is timed to specific moon phases, but the mechanisms for sensing moon phases are incompletely understood. Here the authors report that an ancient, light-sensitive protein L-Cryptochrome in a marine bristle worm can discriminate between sun- and moonlight, enabling the animals to properly decode moon phases.

Camera-type eyes in vertebrates and cephalopods are striking examples of parallel evolution of a complex structure. While comparisons have focused on these two groups, camera-type eyes with likely high functionality are also found in other invertebrate phyla with simpler brains. Employing single-cell RNA sequencing, we identify neurogenic cells in the adult eyes and brain of the marine annelid worm Platynereis dumerilii . Distinct neural stem cells in the camera-type adult eyes, located at the edge of the cup-shaped retina, and adjacent to the glass body/lens, produce radial lines of cells, reminiscent of stem cells in ciliary marginal zones of vertebrate eyes exhibiting life-long growth. Normal proliferation in the eye depends on ambient light, a phenomenon that depends on the integrity of the photoreceptor gene c-opsin1 , which is present in emerging rhabdomeric photoreceptors, and impacts on their differentiation. During reproductive maturation, proliferation in the eye as well as the entire brain sharply declines, while cells upregulate molecular characteristics of mammalian adult neural stem cell quiescence. Our data provide insights into the development and modulation of annelid head and brain cells, revealing similarities and differences to vertebrate eye development, neurogenesis and brain plasticity. Marine worms possess camera-type eyes. Here they show that the growth of marine annelid eyes depends on a stem cell system reminiscent of vertebrate eyes. Moreover, eye development seems to be tuned by a light-sensitive opsin known from vertebrate vision.

Organisms use endogenous clocks to anticipate regular environmental cycles, such as days and tides. Natural variants resulting in differently timed behaviour or physiology, known as chronotypes in humans, have not been well characterized at the molecular level. We sequenced the genome of Clunio marinus , a marine midge whose reproduction is timed by circadian and circalunar clocks. Midges from different locations show strain-specific genetic timing adaptations. We examined genetic variation in five C. marinus strains from different locations and mapped quantitative trait loci for circalunar and circadian chronotypes. The region most strongly associated with circadian chronotypes generates strain-specific differences in the abundance of calcium/calmodulin-dependent kinase II.1 (CaMKII.1) splice variants. As equivalent variants were shown to alter CaMKII activity in Drosophila melanogaster , and C. marinus ( Cma )-CaMKII.1 increases the transcriptional activity of the dimer of the circadian proteins Cma- CLOCK and Cma- CYCLE, we suggest that modulation of alternative splicing is a mechanism for natural adaptation in circadian timing. Genomic and molecular analyses of Clunio marinus timing strains suggest that modulation of alternative splicing of Ca2+/calmodulin-dependent kinase II represents a mechanism for evolutionary adaptation of circadian timing. Night and day habits of a sea midge Kristin Tessmar-Raible and colleagues report the genome of Clunio marinus , a marine midge whose reproduction is timed to the tides by circadian and circalunar clocks. To identify genetic variation associated with timing differences, the authors report genetic mapping in a selection of C. marinus strains with a range of circadian and circalunar timing. They suggest that circalunar and circadian timing are regulated by separate pathways, do not find involvement of core clock genes, and implicate calcium/calmodulin-dependent kinase II.1 in the regulation of circadian timing.

Many species synchronize their physiology and behavior to specific hours. It is commonly assumed that sunlight acts as the main entrainment signal for ∼24-h clocks. However, the moon provides similarly regular time information. Consistently, a growing number of studies have reported correlations between diel behavior and lunidian cycles. Yet, mechanistic insight into the possible influences of the moon on ∼24-h timers remains scarce. We have explored the marine bristleworm Platynereis dumerilii to investigate the role of moonlight in the timing of daily behavior. We uncover that moonlight, besides its role in monthly timing, also schedules the exact hour of nocturnal swarming onset to the nights’ darkest times. Our work reveals that extended moonlight impacts on a plastic clock that exhibits <24 h (moonlit) or >24 h (no moon) periodicity. Abundance, light sensitivity, and genetic requirement indicate that the Platynereis light receptor molecule r-Opsin1 serves as a receptor that senses moonrise, whereas the cryptochrome protein L-Cry is required to discriminate the proper valence of nocturnal light as either moonlight or sunlight. Comparative experiments in Drosophila suggest that cryptochrome’s principle requirement for light valence interpretation is conserved. Its exact biochemical properties differ, however, between species with dissimilar timing ecology. Our work advances the molecular understanding of lunar impact on fundamental rhythmic processes, including those of marine mass spawners endangered by anthropogenic change.

As part of our Q&A series, Genome Biology spoke to four scientists about their personal experiences as parents in their careers to highlight the challenges of researchers having children and the support they need in this regard. Our participants also included a couple (Kristin Tessmar-Raible and Florian Raible), as we were interested to know whether both parents being active researchers can have an impact. One of our participants wishes to remain anonymous.

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.

It is yet unknown when and in what form the central nervous system in Bilateria first came into place and how it further evolved in the different bilaterian phyla. To find out, a series of recent molecular studies have compared neurodevelopment in slow-evolving deuterostome and protostome invertebrates, such as the enteropneust hemichordate Saccoglossus and the polychaete annelid Platynereis. These studies focus on the spatially different activation and, when accessible, function of genes that set up the molecular anatomy of the neuroectoderm and specify neuron types that emerge from distinct molecular coordinates. Complex similarities are detected, which reveal aspects of neurodevelopment that most likely occurred already in a similar manner in the last common ancestor of the bilaterians, Urbilateria. This way, different aspects of the molecular architecture of the urbilaterian nervous system are reconstructed and yield insight into the degree of centralization that was in place in the bilaterian ancestors.