Nematode-Trapping Fungi Eavesdrop on Nematode Pheromones.

Howard Hughes Medical Institute and Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.
Current biology: CB (Impact Factor: 9.92). 12/2012; DOI: 10.1016/j.cub.2012.11.035
Source: PubMed

ABSTRACT The recognition of molecular patterns associated with specific pathogens or food sources is fundamental to ecology and plays a major role in the evolution of predator-prey relationships [1]. Recent studies showed that nematodes produce an evolutionarily highly conserved family of small molecules, the ascarosides, which serve essential functions in regulating nematode development and behavior [2-4]. Here, we show that nematophagous fungi, natural predators of soil-dwelling nematodes [5], can detect and respond to ascarosides. Nematophagous fungi use specialized trapping devices to catch and consume nematodes, and previous studies demonstrated that most fungal species do not produce traps constitutively but rather initiate trap formation in response to their prey [6]. We found that ascarosides, which are constitutively secreted by many species of soil-dwelling nematodes, represent a conserved molecular pattern used by nematophagous fungi to detect prey and trigger trap formation. Ascaroside-induced morphogenesis is conserved in several closely related species of nematophagous fungi and occurs only under nutrient-deprived conditions. Our results demonstrate that microbial predators eavesdrop on chemical communication among their metazoan prey to regulate morphogenesis, providing a striking example of predator-prey coevolution. We anticipate that these findings will have broader implications for understanding other interkingdom interactions involving nematodes, which are found in almost any ecological niche on Earth.

  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: In a recent paper, we reported the isolation and surprising effects of two new bacterial pathogens for Caenorhabditis and related nematodes. These two pathogens belong to the genus Leucobacter and were discovered co-infecting a wild isolate of Caenorhabditis that had been collected in Cape Verde. The interactions of these bacteria with C. elegans revealed both unusual mechanisms of pathogenic attack, and an unexpected defense mechanism on the part of the worm. One pathogen, known as Verde1, is able to trap swimming nematodes by sticking their tails together, resulting in the formation of "worm-star" aggregates, within which worms are killed and degraded. Trapped larval worms, but not adults, can sometimes escape by undergoing whole-body autotomy into half-worms. The other pathogen, Verde2, kills worms by a different mechanism associated with rectal infection. Many C. elegans mutants with alterations in surface glycosylation are resistant to Verde2 infection, but hypersensitive to Verde1, being rapidly killed without worm-star formation. Conversely, surface infection of wild-type worms with Verde1 is mildly protective against Verde2. Thus, there are trade-offs in susceptibility to the two bacteria. The Leucobacter pathogens reveal novel nematode biology and provide powerful tools for exploring nematode surface properties and bacterial susceptibility.
    01/2014; 3(1):e27939. DOI:10.4161/worm.27939
  • [Show abstract] [Hide abstract]
    ABSTRACT: A bacterial strain YMF 3.175 was identified as Alcaligenes faecalis based on its 16S rRNA sequence. Seven compounds including 1,2-benzenedicarboxylic acid bis(2α-methylheptyl) ester (1), cyclo(L-Pro-L-Val) (2), cyclo(Gly-L-Pro) (3), 3-pyridinecarboxylic acid (4), cyclo(L-Pro-L-Tyr) (5), adenosine (6) and L-Val (7) were obtained from the extracts of fermentation broth of this bacterium. Their structures were elucidated on the basis of spectroscopic data. All compounds were assayed for antibacterial activity and the activity of inducing trap formation in nematophagous fungus Arthrobotrys oligospora. Compounds 1, 3 and 6 showed activity against Escherichia coli and Staphylococcus aureus. Compound 7 induced trap formation in A. oligospora.
    Applied Biochemistry and Microbiology 01/2015; 51(1). DOI:10.1134/S0003683815010172 · 0.66 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: In their natural habitat, bacteria are consumed by bacterivorous nematodes; however, they are not simply passive preys. Here we report a defensive mechanism used by certain bacteria to mobilize nematode-trapping fungi to kill nematodes. These bacteria release urea, which triggers a lifestyle switch in the fungus Arthrobotrys oligospora from saprophytic to nematode-predatory form; this predacious form is characterized by formation of specialized cellular structures or 'traps'. The bacteria significantly promote the elimination of nematodes by A. oligospora. Disruption of genes involved in urea transport and metabolism in A. oligospora abolishes the urea-induced trap formation. Furthermore, the urea metabolite ammonia functions as a signal molecule in the fungus to initiate the lifestyle switch to form trap structures. Our findings highlight the importance of multiple predator-prey interactions in prey defense mechanisms.
    Nature Communications 12/2014; 5:5776. DOI:10.1038/ncomms6776 · 10.74 Impact Factor