The morphological development of these traps is the key indicator of their switch from saprophytic to predacious lifestyles. Here, the genome of the nematode-trapping fungus Arthrobotrys oligospora Fres. ATCC was reported. The genome contains
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To study the molecular basis for predator-prey coevolution, we investigated how Caenorhabditis elegans responds to the predatory fungus Arthrobotrys oligospora. Gas-chromatographic mass-spectral analyses of A. One compound, methyl 3-methylbutenoate MMB additionally triggered strong sex- and stage-specific attraction in several Caenorhabditis species. Furthermore, when MMB is present, it interferes with nematode mating, suggesting that MMB might mimic sex pheromone in Caenorhabditis species.
Forward genetic screening suggests that multiple receptors are involved in sensing MMB. Response to fungal odors involves the olfactory neuron AWCs. We propose that A. Predation, in which individuals of one species predators kill and consume the biomass of individuals of another species prey Abrams, , imposes a strong selective pressure on both predators and prey.
To minimize the risk of being eaten, prey have often evolved specific behaviors and strategies such as camouflage, avoidance, mimicry, and tonic immobility to increase their chance of survival. In turn, predators also evolved enhanced predatory strategies to secure food sufficient to survive and reproduce, giving rise to an evolutionary arms race between predator and prey Dawkins and Krebs, While most carnivores are animals, examples of predacious plants and fungi exist.
Venus flytraps, sundews and pitcher plants acquire some or most of their nutrients from trapping and consuming insects, a feature that evolved in response to nitrogen limitation Darwin, Many fungi that grow in nitrogen-poor environments have likewise evolved carnivorism and nematodes, being the most numerically abundant animals on earth, conveniently became the prey Barron, ; Nordbring-Hertz, This predatory lifestyle has independently evolved multiple times among different fungal lineages including Zygomycetes, Ascomycetes and Basidiomycetes Barron, ; Liou and Tzean, ; Yang et al.
Nematode-trapping fungi depend on their elaborate traps to prey on nematodes. However, the majority of the nematode-trapping fungi do not constitutively generate these trapping structures; trap-morphogenesis is only triggered by the presence of nematodes Pramer and Stoll, This suggests that trap-formation might be a highly energy-consuming process and that, to conserve energy, these fungi have evolved to sense signals from nematodes, which indicate the presence of prey.
One such signal is the group of nematode pheromones, ascarosides. These pheromones regulate various aspects of behavior and development in C. Since the nematode-trapping fungi have clearly evolved the ability to eavesdrop on nematode communication, we wondered whether the nematodes also sense and respond to their fungal predators.
For example, Pseudomonas aeruginosa triggers an aversive learning behavior, while another pathogen Bacillus nematocida attracts C. Bacterial secondary metabolites are able to modulate the signaling and the protective lawn-avoidance behavior in C. By contrast, little is known about how C. Many prey are known to begin fleeing when they sense a possible predator, while many predators are also known to attract their prey Haynes et al.
Therefore, we investigated the behavioral and molecular basis for how C. Here, we show that C. We identified several odorants produced by A. Through genetic screens and single-cell transcriptome analyses of the AWC neuron, we identified the potential chemosensory receptors that were expressed in this neuron, which is involved in sensing some of these fungal odors. Our study shows that in order to catch its nematode prey, A. To study how C.
We designed a four-point chemotaxis assay. The number of immobilized worms in each of the quadrants was counted and their chemotaxis index Bargmann et al. We found that the adult C.
This strong attraction was only observed in the adult animals; dauers and the L1 larvae exhibit much weaker attraction to A. A Schematic representation of the 4-point chemotaxis assays and the formulation used to calculate the chemotaxis index CI. C Speed of wild-type C. D Many Caenorhabditis nematodes and the more distant Panagrellus redivivus, Pristionchus pacificus, and Bursaphelenchus xylophilus were attracted to A. E SEM image of C.
To investigate whether the attraction towards A. We observed significant attraction toward A. We thus further tested three additional nematode species that are more phylogenetically distant from C. Like C. We found that all three of these additional species were also attracted to A. To determine whether these diffusible nematode-attracting compounds were soluble or volatile, we designed another version of the chemotaxis assay using three-division Petri dishes.
In this assay, A. We let the nematodes move freely for 2 hr, after which their chemotaxis index was determined by counting the number of worms that had migrated to the sectors with or without the fungal culture Figure 2A.
We still observed significant attraction of C. A Schematic representation of the volatile chemotaxis assays in which A. The CI was calculated based on the formula presented. We next sought to identify the C. There are 32 sensory neurons present in the amphid, phasmid and inner labial organs of C.
For some of these neurons, their functions have been studied in detail Bargmann, To determine whether genes known to play a role in chemotaxis are required for sensing A. We found that che-1 , a gene required for ASE neuron identity and function, was dispensable for A. We thus laser-ablated both AWC neurons in C. To understand how A. Solid-phase microextraction SPME was used to sample headspace volatiles from vials containing medium inoculated with A. Five compounds present only in samples containing A.
To examine whether these A. DMDS has been identified from many bacteria Tomita et al. We found that truffle oil was very attractive to C. These results indicate that several A. The total detector response is indicated by the intensity of red in the chromatogram. Black dots represent discrete elution peaks identified during data processing shown for a signal-to-noise threshold of The elution peaks labeled 1—5 represent compounds that were detected only in A.
B Chemotaxis assays of A. The MMB preference index was calculated according to the formula in Figure 1. E Chemotaxis plot showing C. One of the identified odorants, MMB, was highly attractive to C.
When varying doses were tested for elicited responses, MMB attracted C. Moreover, when C. To examine whether MMB is indeed a genuine molecule naturally produced by A. If the A. Indeed, we found that when C. This reduction in chemotaxis was odorant-specific, as opposed to a global reduction in chemotaxis, as A. Having demonstrated that the AWC neurons are required for attraction towards A.
We then measured the AWC on activity in response to different odorants via a microfluidic device the olfactory chip Chronis et al. The AWC on neurons are known to respond to odor removal Chalasani et al.
We observed a strong activity in the AWC on neuron triggered by several A. To test if the activation of the AWC on neuron was a primary response, we also imaged the AWC on activity in an unc background. Mutations of unc impair the priming of presynaptic vesicles for release, either impairing or completely blocking synaptic transmission Richmond et al.
AWC on neurons were still strongly activated by MMB removal in an unc mutant background, suggesting that this activation is likely to be a direct chemosensory response to MMB Figure 4B. Our data suggest that the AWC neurons sense A. We thus hypothesized that mutants defective in AWC neuron functioning would exhibit lower predation by A. To address this hypothesis, A. After traps had emerged from A. Survival rates of C. We found that the majority of the wild-type animals were trapped by A.
These results indicate that C. MMB potently attracted C. To investigate why adult hermaphrodites were so attracted to this odor, we further examined the chemotaxis behavior in different developmental stages of C. We found that attraction to MMB was both sex- and developmental stage-dependent, as L1 larvae, dauers, and the male animals did not exhibit strong attraction to this odor Figure 5A. Furthermore, when we tested MMB attraction in other Caenorhabditis species, we found that MMB was highly attractive to adult females but repulsive to males in the gonochoristic species such as C.
Therefore, we monitored the mating behavior of C. We chose this species as we found that it has a highly robust and reproducible mating behavior Figure 5C. Furthermore, if the female animals were pre-exposed to MMB odor for an hour before testing, mating efficiency also dramatically decreased Figure 5C.
In contrast, if mineral oil solvent control or diacetyl another food odor attractive to C. A Responses of C. B Responses of Caenorhabditis sp.
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Arthrobotrys oligospora was discovered in Europe in by Georg Fresenius. This fungus reproduces by means of 2-celled, pear-shaped conidia , in which the cells are of unequal size with the smaller cell nearer to the attachment point on the conidiophore. Predation of nematodes occurs in low nitrogen environments,  as the nematode becomes the main nitrogen source for the fungi. A full net is not needed to catch nematodes as smaller nematodes can be caught with a single loop. A substance found in paralyzed nematodes was found to be capable of paralyzing healthy nematodes,   and it was later determined that a paralyzing substance, Subtilisin A serine protease ,  is excreted into nematode. Not all nematodes are caught by the net as the nematode needs to be in contact with the net for a short period of time in order for adhesion to occur.
Please note that this copy of the genome is not maintained by the author and is therefore not automatically updated. Nematode-trapping fungi are a heterogeneous group of organisms broadly distributed in terrestrial and aquatic ecosystems. These fungi are capable of developing specific trapping devices such as adhesive networks, adhesive knobs, and constricting rings to capture nematodes and then extract nutrients from their nematode prey. Most nematode-trapping fungi can live as both saprophytes and parasites.