- Open Access
The worm in the world and the world in the worm
© Blaxter and Denver; licensee BioMed Central Ltd. 2012
- Received: 6 June 2012
- Accepted: 21 June 2012
- Published: 25 June 2012
Caenorhabditis elegans is a preeminent model organism, but the natural ecology of this nematode has been elusive. A four-year survey of French orchards published in BMC Biology reveals thriving populations of C. elegans (and Caenorhabditis briggsae) in rotting fruit and plant stems. Rather than being simply a 'soil nematode', C. elegans appears to be a 'plant-rot nematode'. These studies signal a growing interest in the integrated genomics and ecology of these tractable animals.
See research article http://www.biomedcentral.com/1741-7007/10/59
- Nematode Population
- Soil Nematode
- Beneficial Mutation
- Mushroom Compost
- Compost Heap
While often called a 'soil nematode', C. elegans has rarely been isolated from soils . Sydney Brenner's C. elegans, the iconic N2 strain, came from mushroom compost in Bristol, UK. Like many related nematodes, C. elegans can enter a facultative diapause stage, the dauer, in response to crowding and lack of food. A modified third stage larva, the dauer can survive without feeding for months (compared to the few days of a normal nematode's life), and is resistant to desiccation and other environmental stresses. Dauers can be isolated from compost heaps and other environments rich in rotting vegetation and are commonly found associated with arthropods (woodlice and pillbugs) and molluscs (snails and slugs). It is likely that these invertebrates are used as transport hosts for dispersal to new food sources. Dauers can be isolated from compost heaps and other environments rich in rotting vegetation and are commonly found associated with arthropods (woodlice and pillbugs) and molluscs (snails and slugs). It is likely that these invertebrates are used as transport hosts for dispersal to new food sources. New wild strains can be established from dauers, as the vast majority of individuals will be hermaphrodites capable of founding a dynasty. While useful, dauer-derived isolates are uninformative of the feeding ecology of the species, the dynamics of the lifecycle or mating strategies in the wild.
Several hundred C. elegans strains have been isolated from all continents save Antarctica, and even from isolated islands such as Hawai'i, largely from compost or transport hosts. There is little geographical structure to global C. elegans populations, suggesting extensive dispersal, likely through human agency. Genomic analyses of natural polymorphism patterns in these global strains reveal that while some (for example, those from Hawai'i) are very different from all others, most share large blocks of their chromosomes in a striking mosaic pattern . This is unexpected, and suggests that the pattern of lifecycle history of the species likely includes frequent events of isolation by distance and founding of new populations by small numbers of related nematodes, and less common events of crossing between distinct evolutionary lineages. This study also revealed strong selective sweep events in C. elegans, presumably driven by selection acting on one major, beneficial mutation that drags along large chromosome blocks with it. But what is the ecological context of beneficial mutations in C. elegans? Where does the rare sex happen? Where are the breeding populations of C. elegans to be found? Until these questions are answered, the growing program of research on the population genetics and evolutionary genomics of C. elegans  will lack power and reach.
Few researchers would need much persuading to take a break from the lab or office on a late summer afternoon, and picnic in an idyllic, ancient orchard in the quiet countryside near Paris. What motivated Marie-Anne Félix's visits to the orchards of Orsay and Santeuil, however, was the opportunity to track for the first time robust, proliferating populations of C. elegans (and the related Caenorhabditis briggsae) in the wild. She and her lab team returned to survey the orchards for four seasons, and also examined additional rotting fruit and plants for Caenorhabditis across France, and are now able to report on the ecology of these populations .
C. elegans was found in rotting fruits of many kinds, and also in the rotting stems of herbaceous plants. It was frequently found with C. briggsae, and both species could be found in the same fruit. The nematodes were surprisingly common (20% of rotting apples from Orsay harbored nematodes) and showed reproducible seasonal changes in abundance. The rotting fruit and stems often contained many hundred animals, and all life stages were present, including rare males. As might be predicted from laboratory knowledge of the temperature preferences of the two species, C. briggsae was commoner in the warmth of the summer, and C. elegans in the cooler autumn. Félix and Duveau carried out competition experiments to show that indeed Orsay and Santeuil C. briggsae outcompeted co-isolated C. elegans at 25°C, while the situation was reversed at 15°C. Caenorhabditis were not detected in soils, other than under the rotting fruit, or from rotting fruit yet to fall from the trees, but were isolated from molluscs and arthropods associated with the rotting food sources. It remains to be tested whether these are transport hosts for the nematodes. Importantly, it was possible to return to the same site repeatedly and recover animals each time.
So, rather than the monoxenic environment of the agar plate, it is rich habitats like a rotting apple that C. elegans' chemosensory system has evolved to process. C. elegans lives in a complex ecosystem of bacteria, fungi, slime moulds, hexapod arthropods (adults and larvae), mites, isopods, millipedes, pulmonate molluscs, lumbricid earthworms and other nematode species exploiting this seasonal resource.
C. elegans has a fully functioning immune system, with both anti-cellular (bacterial, fungal) and anti-viral arms intact. In the laboratory, in the absence of knowledge of natural pathogens, these systems have been challenged with exotic ones, such as the agents of human disease. C. elegans can be killed by many bacterial species, sometimes through direct toxic effect but also via interference with efficient processing of food . In the laboratory one of the hallmarks of pathogenic interaction between a bacterium and C. elegans is the proliferation of bacteria within the gut. The species that do this avoid lysis in the nematodes' pharyngeal grinder, and are resistant to digestion. Interestingly, Félix and Duveau  found many instances of apparently healthy nematodes with distended intestines full of bacteria and yeasts. Whether this is a nutritive (C. elegans is deficient in sterol synthesis and must obtain sterols from food: this may be derived from yeasts) or a morbid interaction remains to be tested. However, fungal pathogens were detected, including some species that produce invasive spores, and others that make nematode-trapping rings and adhesive hyphal traps. As previously described by Félix and colleagues, many nematodes were infected with microsporidia , and the first-ever nematode viruses were described from these orchards only last year . Killer bacteria were also isolated, including strains that can digest even the resistant cuticle of the nematodes.
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