Nutritional dynamics in fungus-growing termites: Integration of biological nitrogen fixation and microbial amino acids

1. Termites are pivotal ecosystem engineers in African savanna ecosystems where they significantly contribute to nutrient cycling and facilitate the success of many other organisms. Termites can also introduce atmospheric nitrogen into terrestrial cycling via symbiotic nitrogen-fixing gut bacteria and potentially through fungus gardens maintained by the fungus-growing (Macrotermitinae) species.

2. In termite fungus gardens, a variety of microorganisms, including the symbiotic Termitomyces fungus and various bacteria, break down lignocellulose and recycle organic nitrogen from dead plant matter. However, the specific roles of these fungal and bacterial symbionts in the nutrition of termite hosts are not yet fully understood.

3. Here, we investigate nutritional interactions between Kenyan Macrotermes michaelseni termites and their symbiotic fungi and bacteria using compound-specific stable isotope analyses (δ¹³C and δ¹⁵N) of amino acids (CSIA-AA).

4. Microbial resource utilization varies across termite castes. Essential amino acids (EAAs) in eggs and larvae primarily originate from fungi (50%–67%), whereas bacterial contributions are most pronounced in workers (22%) and soldiers (16%–24%).

5. The amino acid δ¹⁵N patterns indicate that biological nitrogen fixation occurs in both termite guts and their fungus gardens, and the fixed nitrogen heavily affects the amino acid δ¹⁵N values, especially in eggs and larvae. Concurrently, the relatively modest proportion of bacterially synthesized EAAs in the eggs and larvae (<11%) suggests that the fixed ammonium is largely assimilated into amino acids within fungal or termite host cells.

6. These findings underscore the intricate collaborative interactions among bacterial, fungal and insect metabolisms that support the protein supply within this symbiotic system. These interactions may have broader implications for introducing novel atmospheric nitrogen into nutrient-deficient savanna ecosystems.