Journal Article

Combined transcriptome and proteome profiling reveals specific molecular brain signatures for sex, maturation and circalunar clock phase

Schenk, Sven, Hartl, Markus, Bannister, Stephanie C, Tessmar-Raible, Kristin, von Haeseler, Arndt, Raible, Florian, Gerner, Christopher, Anrather, Dorothea, Sedlazeck, Fritz J, Minh, Bui Quang, Bileck, Andrea

2019

Overview

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.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Annelida - genetics / Bioinformatics / Brain - metabolism / chronobiology / Circadian Clocks - genetics / Circadian rhythms / Corals / development / Ecology / Female / Gene expression / Genes / Laboratories / Light / Male / marine biology / Marine organisms / Neuroscience / Ontology / Phylogeny / Proctolin / Proteins / Proteome - metabolism / Proteomes / Proteomics / Sex differentiation / sexual differentiation / Sexual Maturation - genetics / Signal Transduction - genetics / Tools and Resources / Transcriptome - genetics / transcriptomics