The tiny marine ragworm Platynereis dumerilii was first used as a laboratory organism in order to investigate the dependence of its reproduction cycle on the phases of the moon. Recent work carried out by Detlev Arendt at the EMBL in Heidelberg and other researchers is transforming the worm into an evo-devo research model, in particular with regard to the development of its eyes and central nervous system.
When molecular biologists talk about "the worm", they are normally referring to Caenorhabditis elegans. C. elegans is a tiny nematode (threadworm) which is equally as important for science as Drosophila melanogaster ("the fly") or Mus musculus ("the mouse"). The amazing successes of evolutionary developmental biology (evo-devo), including for example the discovery of the Hox genes which show that worms, flies, mice, etc. have structural principles and genetic regulatory mechanisms in common despite having very different blueprints, have led many a researcher to take Jacques Monod's famous bon mot "What is true for E. coli is also true for the elephant" almost too literally. The truth is that important scientific breakthroughs are often obtained unexpectedly while investigating less well-known organisms.
This article focuses on another worm that is much less well known among molecular biologists. This worm has certain characteristics that might lead to it becoming a new model organism for basic evo-devo research issues. Platynereis dumerilii is an inconspicuous marine ragworm that is currently being investigated in around a dozen laboratories around the world, including the laboratory of Detlev Arendt at the European Molecular Biology Laboratory (EMBL) in Heidelberg.
Despite being less known, Platynereis dumerilii (P. dum.) is far from being a new element in the scientific world. The first publication that featured Platynereis dumerilii (P. dum.) listed in PubMed (NCBI) was published by zoologist Carl Hauenschild in 1951, and the first scientific description was published as early as 1833. The worm strains now being used in laboratories are, in the majority of cases, progeny of marine worms caught by Hauenschild in the Gulf of Napoli off the coast of the city of Ischia. The genus Platynereis also includes numerous other species whose breeding biology and conditions differ from that of P. dum. During his time as professor at the universities of Freiburg and Braunschweig, Hauenschild introduced the use of this organism in practical zoology courses for the study of microscopic anatomy and embryonic development. Together with Prof. Albrecht Fischer (who is now retired from his position at the University of Mainz), Hauenschild wrote a monograph about P. dum. Fischer was also the co-initiator of the "Platynereis dumerilii homepage" (www.platynereis.de) which is now maintained by the Institute of Zoology at the University of Gießen (Prof. Dr. Adriaan Dorrestejn).
P. dum. belongs to the class Polychaeta (paddle-footed annelids and polychaetes) which are part of the phylum Annelida (annelids, segmented worms). There are more than 10,000 annelid species, including the well-known earthworms, leeches and the sandworms found in mudflats. According to current systematics, the annelids are not closely related to the nematodes, the category to which Caenorhabditis belongs; it is assumed that the so-called Urbilaterians that lived in the late Precambrian are the last common ancestors of these two animal groups. The Urbilaterians are most likely the ancestors of all other "higher" animals.
Hauenschild and other researchers after him were particularly fascinated by P. dum.’s ability to precisely regulate its reproduction rhythm according to the phases of the moon. The light of the full moon determines (in its role as zeitgeber) the maturation process of the sex cells in adult animals. Exactly 14 days after maturation – at new moon, four hours after sunset – the otherwise soil-dwelling worms float to the surface of the sea where they synchronously release eggs and sperm, and the worms burst and die in the process. The sex organs develop in the abdominal cavity of the worms and have no external exit. The worm, which has an average lifespan of seven months and reaches a length of around 3 – 4 cm, is therefore only able to reproduce once.The lunar periodicity can be reproduced in the laboratory by accurately regulating the light conditions - under natural conditions this is a normal 24-hour day-night rhythm, superimposed by a 28-day moon cycle which can be simulated with a weak 15-Watt light bulb. For experimental purposes, the researchers can modulate the artificial moon phases as external impulse generator, and thus the hormone-dependent differentiation processes that lead to the maturation of the gonads and the subsequent spawning of the worms. The moonlight still exerts its effect even after the four eyes of adult worms are destroyed. The zoologist Dr. Kristin Tessmar from the Max Perutz Laboratories at the University of Vienna assumes that special large cells act as sensors in the (transparent) head of the worm, which respond to the strength of the light, but not to its direction. The lunar periodicity of reproduction became famous thanks to another polychaete, the palolo worm, which is found in tropical coral reefs. Every year, mass spawning occurs at a particular day and a particular site in the sea, enabling the natives of Samoa, for whom palolo worms are a culinary delicacy, to scoop the worms from the sea’s surface with a net.
The palolo worm from Samoa
In the 1890's edition of Meyers Konversations-Lexikon, a major German encyclopaedia that existed between 1839 and 1984, the spawning of the palolo worms of Samoa is described under the keyword "Würmer" (worms) in a comprehensive and amusing way (further information at www.retrobibliothek.de). Short extract: "Suddenly, towards dawn (on the 2nd day after the onset of the last quarter of the moon in November), the long worms, which fluoresce in a wide range of colours, crawl out from numerous crevices and holes in the coral reef and spawn to the surface. The entire sandy beach is soon covered with a teeming layer of worms. Cheering loudly, young and old people wade into the milling mass, scoop up all the worms they can, filling the pots they have with them. There is no time to be lost because as soon as the sun's first rays hit the surface of the sea, the animals return to their crevices and gaps as if they were drawn down into the water by demonic forces. They disappear within a few minutes. The natives then joyfully return to their families with their successful harvest."
The "half-worms", which the natives of Samoa find so tasty, are around 25 - 30 cm long and around 1 - 2 cm thick. However, they are unusual worms. The palolo worms and their close relatives have developed a clever strategy which, in total contrast to P. dum, enables them to undergo several reproduction cycles. The rear ends of the palolo worms' bodies, the parts that contain the eggs and sperm, drop off. This part of the body, which has its own groups of photoreceptors, then floats to the surface of the water, releases sperm and eggs and dies. The front part of the body, including the animal's head, brain, etc. is not involved in reproduction; it remains on the sea bed and regenerates the rear part that has dropped off. During the next spawning period, a new rear end, containing sperm and eggs, is dropped off again and released to the sea surface.
Dr. Detlev Arendt's team at the EMBL in Heidelberg is investigating the structure and function of the eye spots in Platynereis larvae. Platynereis larvae eyes are the simplest eyes in the animal kingdom, consisting of only two cells, a photoreceptor cell and a pigment cell. The photoreceptor detects light and converts it into an electrical signal that is directly transmitted through its neural projection to a band of cilia, which the ragworms use to move around. The pigment cell absorbs light and casts a shadow over the photoreceptor. The shape of this shadow varies according to the position of the light source and changes the way the cilia beat. The larvae feed on plankton and, together with many other plankton organisms, migrate vertically in the ocean in response to the rhythm of time: During the day, the larvae move towards the light (positive phototaxis); at night, the larvae return to greater depths. This is the largest biomass transport in the world.
"We assume that the first animal eyes developed for this particular reason," said Arendt. "Insights into phototaxis provide us with information about the evolution of the eyes." The researchers have used molecular fingerprinting to show the relationship between the ciliary photoreceptor and the photoreceptors (rods and cones) in the retina of vertebrates. Dr. Gáspár Jékely, one of Arendt ‘s former co-workers who now heads up his own research group at the Max Planck Institute for Developmental Biology in Tübingen, refers to Platynereis as a living fossil because it still lives in the same environment as its ancestors did millions of years ago and it most likely still has many Urbilaterian characteristics. "By investigating the eye spots of the Platynereis larvae, we will potentially come as close as possible to revealing the evolutionary origin of the eye." Many marine invertebrates have the same phototaxis mechanism. In addition, the researchers have also found different types of neurons in the brain of P. dum., which have both sensory and neurosecretory functions. Their molecular characterisation also revealed surprising parallels with vertebrate cells, in particular with the cells located in the hypothalamus.
The researchers' findings show that the brain of P. dum. contains many cells that were previously only known in vertebrates, with the only difference that they are arranged differently and more simply. It would appear that Platynereis dumerilii is slowly but surely becoming a model organism of evo-devo research, in particular with regard to the evolution of the bilaterian central nervous system.