Inconspicuous ringed worms make it big in the field of developmental biology. Their larvae have a rudimentary nervous system with relatively simple circuits. Research involving ringed worms provides insights into the evolution of neural development as well as giving incentives for the development of practical applications.
Only a handful of animals have become popular and well-studied model organisms in the biosciences, including mice, zebra fish, fruit flies and threadworms. Hardly any marine animals are used. “With the exception of sea urchins, only a few marine animals have been studied in detail and used as laboratory models for developmental biology research,” said Dr. Gáspár Jékely from the Max Planck Institute for Developmental Biology in Tübingen who would like to expand the number of model organisms that can be used for this type of research. He has chosen Platynereis dumerilii, a marine ragworm that belongs to the Annelida phylum, for various reasons, a major one being that Platynereis worms and larvae are easy to breed in the laboratory. “I established our Platynereis cultures when I moved from Heidelberg to Tübingen in 2007. We now have several hundred aquariums and can breed the worms as easily as zebra fish,” Jékely said pointing out that this gives him and his 10 colleagues access to a constant supply of laboratory animals.
Annelids are excellent objects of study for developmental biologists because they have changed very little throughout evolution. “They are kind of living fossils like the coelacanth Latimeria. Platynereis has existed since the Cambrian and has only accumulated limited evolutionary change, which is most likely due to it having continued to live in the same environment as its ancestors 500 million years ago. We can measure how quickly the genes change and have found that Platynereis evolves relatively slowly,” Jékely said.
Platynereis worms and larvae have become so popular in developmental research because they still have many ancestral features. “We can learn many things from this animal, especially as far as the evolution of the nervous system is concerned,” Jékely said. The larvae are excellently suited for studying the swimming motion and swimming depth of Platynereis dumerilii. Platynereis larvae have a ciliary band along their body consisting of thousands of cilia beating coordinately, which they use to propel themselves forward in a helical fashion. Platynereis larvae, which are a marine plankton, can swim freely in open water. The cilia beat with a frequency that keeps the larvae at practically the same location. However, with changing environmental conditions, the larvae swim upwards and downwards to their appropriate water depth. The ability to swim up- and downwards prevents them from being exposed to harmful environmental conditions such as high temperatures or high UV radiation. The larvae regulate the swimming depth by influencing the ciliary beat. When the cilia beat fast and continuously, the larvae swim upwards, and when the cilia stop beating, the larvae sink. The larvae alter their vertical movement according to changes in temperature, light and food supply. However, detailed knowledge about why Platynereis larvae constantly move up and down is not yet available. “Maybe the larvae have “invented” this mechanism as it helps them swim at a specific depth without requiring too much energy. Each ciliary movement has an energy cost,” speculates Jékely.
Platynereis larvae sense different physical environmental conditions such as changes in light and temperature as well as the chemical composition of their environment and alter their movement in the water column accordingly. Changing environmental conditions trigger neuronal signals that regulate ciliary movement. Jékely and his team have found eleven neuropeptides that altered ciliary beat frequency and the rate of ciliary arrest. They also found that the activity of the cilia depended on the quantity and composition of the neuropeptides. “Our experiments have already suggested additive effects; we also found that the effects of inhibitory and excitatory neuropeptides cancelled each other out,” said Jékely. If the signal leads to a movement, the larvae can move in any direction at different speeds. The researchers found that the nervous circuitries responsible for this are built in an unusually simple way: the sensory nerve cells also have motor function, which means that they send the motion signal directly to the ciliary band.
The team from Tübingen clarified and published their findings on the phototaxis of Platynereis in the scientific journal Nature in 2008. Platynereis larvae have two eyespots composed of two cells (a photoreceptor cell and a shading pigment cell); the eyespots are located on either side of the body, which allow the larvae to navigate guided by light. The ingenious thing is that the beat of the cilia enables the larvae to turn around their own axis. “Shining light selectively on one eyespot changes the beating of the adjacent cilia. The resulting local changes in water flow are sufficient to alter the direction of swimming. This leads to a helical forward motion,” explained Jékely, pointing out that this was shown with computer simulations of larval swimming (www.cytosim.org/platynereis/; software can be downloaded free of charge).
As explained above, the two photoreceptor cells control the beating of the cilia. “This is the simplest neuronal circuit that has ever been found. We believe that the cells of the Platynereis eyespot are quite old multifunctional cells in evolutionary terms; the eyespots resemble Darwin’s ‘proto-eyes’, which are considered to be the first eyes to appear in animal evolution. Our investigations provide us with greater details on the development of animal eyes. This helps us to obtain a complete functional model of every step in the development of animal eyes and hence a better idea about the evolution of eyes in general,” Jékely explained. In addition to detailed insights into the evolution of eyes, the results of the researchers from Tübingen also provide ideas for technological innovations. The phototaxic model of the larvae has the potential to be used as a model for underwater robots and navigation strategies in general. Jékely believes that the simplicity of the circuits can provide important impulses for such developments.
The researchers have also gained detailed insights into the chemotactic behaviour of Platynereis larvae. However, Jékely points out that the chemotactic behaviour of Platynereis larvae is different from classical chemotaxis. “Chemotactic behaviour in the true sense of the word does not occur in the ocean; there is too much turbulence in the ocean, which prevents a stable gradient from forming. However, Platynereis larvae possess chemosensory cells that produce neuropeptides with which they regulate cilary movement.” It appears that the cells are able to detect substances that Platynereis larvae feed on, including particles rising up from sea grass and macroalgae. Chemotaxis also plays a role in the development of the larvae into juvenile worms. Under suitable environmental conditions, the larvae sink to the seabed and start to form additional body segments. Adult Platynereis worms have more than 50 segments and live on the ocean floor. The researchers from Tübingen are currently focused on gaining insights into how the successive formation of additional segments is regulated.
Research into the chemotactic behaviour of Platynereis also has practical aspects. Sea urchins and mussels – which are increasingly bred in aquacultures for human consumption – have similarly regulated developmental cycles. Although marine annelids are not really suitable for human consumption, they are nevertheless bred in large numbers in aquacultures. “Large numbers of annelids are used as bait by the Japanese fishing industry and are thus bred in huge numbers. This is a million-dollar business,” Jékely said. From an economic perspective, it would therefore be highly interesting if it were possible to control the development of the worms and adapt production to demand. The researchers assume that the larvae are able to sense changes in light and chemical signals as well as changes in temperature and environmental pressure and that these changes affect the larvae’s lifespan and development. The researchers from Tübingen are also focused on elucidating these issues. Jékely and his team believe that the simple circuitry found in Platynereis larvae may represent an ancestral state in nervous system evolution and have expanded their research to other marine planktonic organisms that also have simple nervous systems.
Jékely’s team has used Platynereis peptides to develop some neuronal antibodies with the aim of studying the anatomy of the nervous systems of other marine organisms. Jékely is convinced that the rapid development of biological methods will help his field of research to make great strides forward. “Genome sequencing is becoming quicker and cheaper; we are also able to cut and edit genes. State-of-the-art methods enable us to create knockout mutations by injecting DNA into annelid eggs. Technological progress enables us to investigate neuronal aspects on the molecular level. I therefore believe that it is high time to start expanding the range of popular model organisms and establish new ones such as Platynereis.”
Further information:Max Planck Institute for Developmental BiologyDr. Gáspár JékelySpemannstr. 35 - 3972076 TübingenE-mail: firstname.lastname@example.orgTel.: +49 (0)7071 601-1310