Identification of attractive odorants released by preferred bacterial food found in the natural habitats of C. elegans.

Soleil E Worthy,Lillian Haynes,Charles J Taylor,Emily Kan,Ryan Ota,Melissa Chambers,Danika Bethune,Elizabeth E Glater,Kevin Chung,Hiroaki Matsunami

doi:10.1371/journal.pone.0201158

Abstract

Food choice is critical for survival because organisms must choose food that is edible and nutritious and avoid pathogenic food. Many organisms, including the nematode C. elegans, use olfaction to detect and distinguish among food sources. C. elegans exhibits innate preferences for the odors of different bacterial species. However, little is known about the preferences of C. elegans for bacterial strains isolated from their natural environment as well as the attractive volatile compounds released by preferred natural bacteria isolates. We tested food odor preferences of C. elegans for non-pathogenic bacteria found in their natural habitats. We found that C. elegans showed a preference for the odor of six of the eight tested bacterial isolates over its standard food source, E. coli HB101. Using solid-phase microextraction and gas chromatography coupled with mass spectrometry, we found that four of six attractive bacterial isolates (Alcaligenes sp. JUb4, Providenica sp. JUb5, Providencia sp. JUb39, and Flavobacteria sp. JUb43) released isoamyl alcohol, a well-studied C. elegans attractant, while both non-attractive isolates (Raoultella sp. JUb38 and Acinetobacter sp. JUb68) released very low or non-detectable amounts of isoamyl alcohol. In conclusion, we find that isoamyl alcohol is likely an ethologically relevant odor that is released by some attractive bacterial isolates in the natural environment of C. elegans.

Highlights

All organisms must find and detect good food sources that promote growth and survival and avoid detrimental food sources that slow growth or cause illness
What natural bacterial isolates does C. elegans prefer? Second, what natural bacterial isolates does C. elegans prefer based on only olfactory cues? Third, what are the volatile chemicals released by these attractive bacteria? We found that C. elegans showed a strong or moderate preference for the odor of six of the eight tested bacterial isolates over E. coli HB101
In this study, we chose to focus on bacterial strains that are non-pathogenic or mildly pathogenic to C. elegans because previous studies have identified attractive volatile odors released by pathogenic bacteria [7,10,16]

Summary

Introduction

All organisms must find and detect good food sources that promote growth and survival and avoid detrimental food sources that slow growth or cause illness. For many organisms, including humans, olfaction is a major way of discriminating among different food types [1]. The nematode C. elegans lives in microbe-rich habitats of rotting fruit and plant matter where they mainly feed on bacteria and likely use olfaction to find bacterial food [2]. It has long been known that C. elegans is attracted to many volatile compounds that are released by bacteria, including alcohols, ketones, aldehydes, esters and amines, and can discriminate among mixtures of volatile compounds released by different kinds of bacteria [3,4,5,6].

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Conclusion