The Natural History of Caenorhabditis Elegans

The Natural History of Caenorhabditis Elegans

Magazine R965 Does Hydra have an associated one of us (M.A.F.) has experienced, microbiome? Yes, it does. Like Primer long years of skimming through soil the human gut, Hydra is home to samples from all corners of the world an array of bacterial residents. The have been frustratingly fruitless. composition of the microbiome for a The natural history Human-made compost heaps are a particular strain of Hydra seems to be relatively reliable source of C. elegans, quite stable. How the microbiome is of Caenorhabditis allowing the first ‘semi-natural’ studies maintained and what it contributes to elegans on the extent and spatial structure the host are important questions that of its genetic diversity, population are starting to be addressed. Hydra Marie-Anne Félix1 dynamics and outcrossing rate. Several is a much simpler model for studying and Christian Braendle2 more years had to elapse before host/microbe interaction than C. elegans was regularly sampled from vertebrate models such as humans In the laboratory, the nematode more undisturbed habitats. Thanks to and mice. Caenorhabditis elegans lives on repeated scouring of various microbe- the surface of nutrient agar in Petri rich samples in diverse habitats, we I’ve heard that Hydra is immortal; dishes, feeding on a lawn of the and others have found C. elegans is that true? It appears so. Daniel uracil auxotroph strain OP50, an and other Caenorhabditis species in Martinez followed 100 adult Hydra Escherichia coli mutant strain. This different types of rotting plant material, for four years, discarding the buds sentence sums up the fundamentals such as fruits, stems and flowers as they were produced. The parental of C. elegans ecology, as most of us (Figure 1). animals did not undergo age-related know it. While over 15,000 articles on Current data thus indicate that senescence. Individual cells die in diverse biological aspects of C. elegans C. elegans is not principally a soil Hydra, but the organism as a whole attest to the worm’s undisputable nematode, but rather a colonizer does not have a fixed life-span. virtues as a major model organism, of various microbe-rich habitats, There is, however, evidence that its biology in the wild remains in particular decaying plant matter. some species of Hydra undergo mysterious. To properly interpret and Improbable as it may seem, rotting senescence following sexual fully understand the available wealth of fruit/plant material thus unites three reproduction. Genes associated with genetic, molecular and other biological major lab model organisms in the same the aging process in other animals observations made in the laboratory, ecological context: Saccharomyces have not yet been examined in Hydra, it will be important to know its natural cerevisiae, Drosophila melanogaster but clearly one would like to know history and to place the species in its and C. elegans. What the three species more in this regard. ecological and evolutionary context. share is a rapid lifecycle, a likely legacy With the aim of connecting the from their boom-and-bust lifestyle Where can I find out more? discoveries that have been made about exploiting ephemeral resources. Chapman, J.A., Kirkness, E.F., Simakov, O., C. elegans biology to its ‘real life’, we Hampson, S.E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P.G., Borman, J., shall discuss recent studies on the Phylogenetic context and Busam, D., et al. (2010). The dynamic genome worm’s natural habitat and population biogeography of Hydra. Nature 464, 592–596. biology, and outline key issues in The genus Caenorhabditis presently Fraune, S., and Bosch, T.C. (2007). Long-term maintenance of species-specific bacterial attaining a modern natural history comprises around 25 described microbiota in the basal metazoan Hydra. of C. elegans. species, of which only seven have Proc. Natl. Acad. Sci. USA 104, 13146–13151. Hydra genome browser: http://hydrazome. been maintained as live or frozen metazome.net/ Natural habitat lab stocks. Their natural habitat Martínez, D.E. (1998). Mortality patterns suggest Where does C. elegans live? Efforts and ecological specificities are very lack of senescence in hydra. Exp. Gerontol. 33, 217–225. to systematically sample C. elegans poorly understood, mainly because Martínez, D.E., Iñiguez, A.R., Percell, K.M., Willner, in nature were initially hampered by many species have been isolated J.B., Signorovitch, J., and Campbell, R.D. the absence of precise ecological only once or twice. The exception is (2010). Phylogeny and biogeography of Hydra (Cnidaria: Hydridae) using mitochondrial and information on the whereabouts of C. drosophilae, which seems to be nuclear DNA sequences. Mol. Phylogenet. this tiny roundworm, which reaches ecologically specialized: this species Evol. 57, 403–410. a length of only 1–2 mm as an adult. has been found on rotten Saguaro Trembley, A. (1744). Mémoires, pour Servir à l’Historie d’un Genre de Polypes d’Eau Douce, The first description ofC. elegans cactus in Arizona, in a phoretic à Bras en Forme de Cornes (Leiden: Jean and and its site of isolation by the French (transport) association with the fly Herman Verbeek). van Leeuwenhoek, A. (1996). The collected letters zoologist Emile Maupas did not Drosophila nigrospiracula, allowing of Antoni van Leeuwenhoek. In The Collected simplify this task: “J’ai rencontré à dispersal between cactus plants. Letters of Antoni van Leeuwenhoek, Volume deux reprises cette espèce dans les Although the Caenorhabditis species XIV, L.C. Palm, ed. (Lisse, Berwyn, PA: Swets and Zeitlinger), pp. 169–173. environs d’Alger: une première fois en forming the ‘Elegans-group’ are Wittlieb, J., Khalturin, K., Lohmann, J.U., mai, la seconde en novembre 1897. morphologically similar, they are highly Anton-Erxleben, F., and Bosch, T.C.G. (2006). Elle vit dans l’humus gras” divergent at the genetic level. To what Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. (“I came twice across this species in degree this divergence is linked to Proc. Natl. Acad. Sci. USA 103, 6208–6211. the surroundings of Algiers: a first time alternative ecological specialization of in May, a second time in November different species remains so far largely 1897. It lives in rich humus”, Maupas unexplored. Department of Biological Chemistry and the Developmental Biology Center University wrote in 1900). From then on, The recent burst of world-wide of California, Irvine, CA 92697-1700, USA. C. elegans was referred to as a soil sampling from rotting plant material *E-mail: [email protected] nematode in the literature. Yet, as has yielded many new Caenorhabditis Current Biology Vol 20 No 22 R966 Proliferation Proliferation develop into adult hermaphrodites on rotting fruit Dispersal on rotting fruit that enter reproductive diapause. In or stem via invertebrate or stem addition, in the adult stage, individuals carrier may promptly stop laying embryos upon food depletion, while the embryos Nictation behaviour remaining in the uterus continue to mature, hatch internally and feed on the decaying mother during the initial larval instars — perhaps a strategy guaranteeing that a small number of internally developing larvae reach the dauer stage. Finally, if starved, C. elegans may also diapause in the L1 stage — the only stage that Adult Adult Embryos Embryos survives freezing over years. Whether this freezing resistance is ecologically Direct Dauer larva Direct d L4 reproductive L1 L2d L4 reproductive L1 L2d d relevant, for example for survival during cycle(s) cycle(s) cold winters in temperate zones, L2 L2 L3 L3 is not known. Many developmental genetic studies Current Biology have investigated dauer formation — a prime example of apparently Figure 1. The life cycle of C. elegans in its natural habitat. adaptive phenotypic plasticity. In the C. elegans proliferates in various types of rotting plant material, such as fruits. Dauer larvae are the stress-resistant, alternative L3 stage, induced by crowding, food depletion and high lab, dauer entry is induced during the temperature. Dauer larvae may actively disperse to colonize new food sources. Alternatively, L1–L2 stages by synergistic effects of their nictation behaviour — standing on their tail on pointy surfaces such as moss leaves and low food concentration, pheromone waving — may allow them to attach to disperse via carriers, such as slugs, snails, isopods or sensation at high population myriapods, until a new food source is encountered, where development resumes. L1–L4, larval densities, and high temperature. This stages; d, dauer larva; L2d, pre-dauer larva in the L2 stage. developmental choice involves sensory regulation through the TGF-ß, insulin species and given a clearer picture details, see http://blog.wormbase. and steroid pathways. Among natural of the distribution of C. elegans and org/?s=sister+prize). isolates of C. elegans, substantial relatives. There are, however, still genetic variation is found in the important geographical sampling Development, diapause and dispersal sensitivity to entering the dauer stage biases — often coinciding with past When well-fed in the laboratory, at in response to given amount of dauer holiday or congress locations of 20°C, C. elegans passes in about 3.5 pheromone or temperature. Exit from zealous C. elegans naturalists. to 4 days through a short embryonic the dauer stage is a key, irreversible C. elegans is cosmopolitan, being developmental period, followed by decision made at the individual level. found on most continents and four juvenile stages (named L1 to L4), Lab studies indicate that high food many isolated islands. It shares the separated by a phase of lethargus concentration and low temperature are temperate regions with two relatives of and moulting. C. elegans, or rather the cues favouring dauer exit, but natural the ‘Elegans group’, C. briggsae (also a reference lab strain N2, can develop cues may differ and are not necessarily facultative self-fertilizing species) and and reproduce at a wide range of symmetric with those for dauer entry.

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