Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey
Abstract
To study the molecular basis for predator-prey coevolution, we investigated how Caenorhabditis elegans responds to the predatory fungus Arthrobotrys oligospora. C. elegans and other nematodes were attracted to volatile compounds produced by A. oligospora. Gas-chromatographic mass-spectral analyses of A. oligospora-derived volatile metabolites identified several odors mimicking food cues attractive to nematodes. One compound, methyl 3-methyl-2-butenoate (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. Single-cell RNA-seq revealed the GPCRs expressed in AWC. We propose that A. oligospora likely evolved the means to use olfactory mimicry to attract its nematode prey through the olfactory neurons in C. elegans and related species.
Additional Information
© 2017 Hsueh et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 24 July 2016; Accepted: 28 December 2016; Published: 18 January 2017. We thank Marie-Anne Felix (IBENS), Cori Bargmann (The Rockefeller University), Ryoji Shinya (Sternberg lab), Vivian Chiu (then in Sternberg lab) and the Caenorhabditis Genetics Center (University of Minnesota) for providing the nematode strains used in this study. We also thank Valerie Knowlton (NCSU) for acquiring the SEM image and Clay Wang (USC) for providing the Aspergillus strains. Michael Milligan (SUNY Fredonia) provided invaluable assistance with GC x GC-TOFMS analyses and Chris Cronin and Sreekanth Chalasani (Salk Institute) provided advices for the calcium imaging set-up. We thank Gladys Medina, Sarah Kim, Chiang Yu Shi and Ka-Naam Heung for providing technical assistance and members of the Sternberg laboratory for helpful discussion. This work was supported by HHMI, with which PWS is an investigator, by the NIH K99 award 1 K99GM108867-1 to YPH, by NIH GM084389 to PWS, and startup funds from Academia Sinica to YPH. RN was supported by T32-GM007616. Author contributions: Y-PH, Conceptualization, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Writing—original draft, Writing—review and editing; MRG, Data curation, Formal analysis, Writing—original draft; EMS, Data curation, Formal analysis, Methodology, Writing—original draft, Writing—review and editing; RDN, C-HL, Data curation, Formal analysis; SG, Data curation, Validation; FCS, Formal analysis, Supervision, Writing—review and editing; PWS, Conceptualization, Resources, Supervision, Funding acquisition, Writing—review and editing. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. The authors declare that no competing interests exist.Attached Files
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Additional details
- PMCID
- PMC5243009
- Eprint ID
- 73619
- Resolver ID
- CaltechAUTHORS:20170123-103744458
- Howard Hughes Medical Institute (HHMI)
- 1 K99GM108867-1
- NIH
- GM084389
- NIH
- Academia Sinica
- T32-GM007616
- NIH Predoctoral Fellowship
- Created
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2017-01-26Created from EPrint's datestamp field
- Updated
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2021-11-11Created from EPrint's last_modified field