Abstract
We present a new perspective for the role of Termitomyces fungi in the mutualism with fungus-growing termites. According to the predominant view, this mutualism is as an example of agriculture with termites as farmers of a domesticated fungus crop, which is used for degradation of plant-material and production of fungal biomass. However, a detailed study of the literature indicates that the termites might as well be envisioned as domesticates of the fungus. According to the “ruminant hypothesis” proposed here, termite workers, by consuming asexual fruiting bodies not only harvest asexual spores, but also lignocellulolytic enzymes, which they mix with foraged plant material and enzymes of termite and possibly bacterial origin. This mixture is the building material of the fungus garden and facilitates efficient degradation of plant material. The fungus garden thus functions as an external rumen for termites and primarily the fungi themselves benefit from their own, and gut-derived, lignocellulolytic enzymes, using the termites to efficiently mix these with their growth substrate. Only secondarily the termites benefit, when they consume the degraded, nitrogen-enriched plant-fungus mixture a second time. We propose that the details of substrate use, and the degree of complementarity and redundancy among enzymes in food processing, determine selection of horizontally transmitted fungal symbionts at the start of a colony: by testing spores on a specific, mechanically and enzymatically pre-treated growth substrate, the termite host has the opportunity to select specific fungal symbionts. Potentially, the gut-microbiota thus influence host-fungus specificity, and the selection of specific fungal strains at the start of a new colony. We argue that we need to expand the current bipartite insect-biased view of the mutualism of fungus-growing termites and include the possible role of bacteria and the benefit for the fungi to fully understand the division of labor among partners in substrate degradation.
Highlights
Mutualistic symbiosis has played a major role in evolution
According to this novel hypothesis fungal enzymes and spores produced in nodules are mixed with the foraged plant material and enzymes of termite and bacterial origin
This mixture initially benefits the growth of the fungus, and facilitates efficient degradation of plant material, to the benefit of the termites in the form of a nitrogen enriched food source
Summary
Mutualistic symbiosis has played a major role in evolution. Through synergy of combined abilities, a mutualistic alliance between two or more species can adapt faster than individual organisms [1]. A symbiosis between a proto-eukaryotic cell and endosymbiotic prokaryotes is at the basis of eukaryotes, which eventually led to protists, plants, fungi and animals [2]. Another example is the symbiosis between plants and arbuscular mycorrhiza, which allowed the colonization of land by plants, fundamentally altering environmental conditions on earth [3]. It is estimated that 20% of all insects are obligatorily associated with symbiotic microorganisms, such as endosymbiotic bacteria and gut bacteria, allowing these groups to specialize on imbalanced food sources [7,8]. We discuss the potential role of bacteria, which have been studied in much less detail, and their potential to mediate host-fungus specificity
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