Fungiculture or Termite Husbandry? The Ruminant Hypothesis

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.

Keywords: Macrotermitinae; Termitomyces; fungus-growing termites; gut microbiota; host-symbiont specificity; lignocellulose; ruminant hypothesis.

Figure 1

Aspects of the mutualism between fungus-growing termites and Termitomyces fungi, using Macrotermes as a model system. (a) Close-up of a fungus garden with multiple asexual fruiting bodies (nodules). The spores survive passage through the termite gut and are mixed with predigested plant material to be deposited as inoculated fresh garden substrate [17,18]; (b) the queen and king in an opened royal chamber; (c) A fungus garden showing freshly-deposited substrate on top (dark), multiple nodules in mature parts (white structures), and degraded lower parts; (d)the inside of a colony showing the interconnected network of chambers that contain fungus gardens, containing a mass of masticated plant substrate in which Termitomyces grows (the fungus comb); (e) Mushrooms of various developmental stages of a colony Macrotermes natalensis; (f) Key aspects of the life cycle of a typical species of fungus-growing termites with horizontal transmission [23]. The fungus is clonally propagated via asexual spores inside the colony [24], which can live for more than 20 years. Dispersal occurs via the yearly production of sexual offspring, independently in termites (alates) and fungi (sexual spores from mushrooms); (g) Patterns of coevolution between fungus-growing termites (left) and their associated Termitomyces fungi (right) [10].

Figure 2

Schematic overview of the composition of secondary plant-cell walls of woody tissue and grasses, which are composed predominantly of lignin, hemicellulose and cellulose. Some of the most important enzymes involved in the degradation of the main polysaccharides into disaccharides and oligosaccharides, which are further degraded to soluble monosaccharides that can be assimilated, are shown.

Figure 3

Alternative hypotheses for the role of the fungus as a source of food, spores and enzymes. (a) According to the acquired enzyme hypothesis, fungi and termites deliver different sets of cellulolytic enzymes, which together degrade the plant material inside the gut; (b) Nodules are an additional protein-rich food source and are used to inoculate the fungus garden; (c) the ruminant hypothesis—here raised—where nodules are a source of food, enzymes and spores. The fungi may deliver the complete set of (ligno)cellulolytic enzymes, or the fungi and termites deliver different, complementary sets.