The scent of earth – a connection between sporulating soil bacteria and springtails
Dr. Paul G. Becher
Associate Professor, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Sweden
Dr. Klas Flärdh
Professor, Department of Biology, Lund University, Sweden
When digging into soil, we uncover the fragrance of earth that many of us associate with gardening, agriculture or a walk in the forest. The earthy smell is so familiar to us and common on our planet that we might not think about it as anything more than a meaningless whiff. However, the volatile compounds we smell often have a biological function for those that release or those that detect the compounds. So, what about that earthy scent of soil? Could it have an ecological significance?
A springtail (Folsomia candida), mounted and ready for elecrtroantennographic detection. Electrodes are then attached to its antennae to detect neurophysiological responses. Photo credit: Béla P. Mólnar, Zoology Department, Plant Protection Institute, Centre for Agricultural Research, Budapest, Hungary.
The smell of soil derives largely from the two characteristic volatile organic compounds (VOCs) geosmin and 2-methylisoborneol, which have long been known to be produced by soil bacteria of the genus Streptomyces. Streptomyces bacteria as a group are known for their ability to produce thousands of specialized metabolites, and they are the source of many of our clinically used antibiotics. Each isolated strain has the ability to produce a subset of perhaps 20-30 different compounds. Despite the huge variability in the spectrum of compounds produced by each strain of Streptomyces, they all have one thing in common: the ability to produce geosmin, and many of them also make 2-methylisoborneol. However, it has remained a mystery why streptomycetes emit these earthy scents and what benefits they may have from it. We postulated that the volatiles emitted by Streptomyces spp. are not only perceived by humans, but also by animals that dwell in or on the ground.
The problem was that we did not know which group of animals to look for as the odor so far was mainly known as off-flavor to humans and aversive smell to Drosophila fruit flies. We therefore went ‘fishing’ in the soil with Streptomyces-baited traps to find out if anything could be attracted to the lure made of sticky cardboards and bacterial cultures. What we collected were springtails (order Collembola) which are small six-legged invertebrates closely related to insects who feed on microbes in soil and detritus.
With this finding we concentrated on the springtail Folsomia candida, which can be reared for laboratory experimentation. We confirmed that F. candida is attracted to the odor of Streptomyces spp., and we also visualized the sensory response by electrophysiological recording from springtail antennae stimulated with geosmin or 2-methylisoborneol. Moreover, in the lab we could see that F. candida was able to use Streptomyces biomass as a food resource. Finding springtails responding to Streptomyces odor was interesting, but it did not yet explain any benefit for the bacteria emitting the VOCs.
A springtail (Folsomia candida) next to Streptomyces biomass (in black). The springtail gut is filled with ingested biomass (in black). Photo credit: Paul G Becher.
An investigation of how the bacteria regulate biosynthetic production of geosmin and 2-methylisoborneol gave us a hint for a possible function. The production of these volatiles was tightly connected to the formation of spores, which are reproductive units formed on the surface of Streptomyces colonies, for example when they run out of nutrients. The spores serve for dispersal and survival of the bacteria when there are adverse environmental conditions. What we found was that genes for geosmin and 2-methylisoborneol production are only expressed when the Streptomyces bacteria make spores. Knowing how the VOC production was integrated into the Streptomyces developmental life-cycle, we hypothesized that the attraction of springtails might have a role in spore dispersal.
We saw that the Streptomyces spores attach remarkably well to the surface (cuticle) of the springtail body. Moreover, when being ingested by the springtails, spores survive passage through the springtail gut and are released in fecal pellets. These two modes of dispersal by springtails is similar to the vectoring of plant reproductive units in other symbiotic relationships, such as the transport of pollen by bees or the dispersal of seeds by birds.
In summary, when Streptomyces bacteria run out of nutrients and sporulate, they emit geosmin and 2-methylisoborneol to attract springtails. The animals feed on the bacterial biomass, and at the same time they help the bacterium to disperse by spreading its spores to new locations. Thus, the smell of soil we may perceive on a walk through the woods is actually part of an ecological interaction between microbes and arthropods that has coexisted for several hundred million years.
Publication: Becher PG, Verschut V, Bibb MJ, Bush MJ, Molnár BP, Barane E, Al-Bassam MM, Chandra G, Song L, Challis GL, Buttner MJ, Flärdh K (2020) Developmentally regulated volatiles geosmin and 2-methylisoborneol attract a soil arthropod to Streptomyces bacteria promoting spore dispersal. Nature Microbiology 5, 821–829. https://doi.org/10.1038/s41564-020-0697-x