Biochemical Basis of Termite Ecological Success

Cockroaches live in eusocial colonies that usually contain a king and a queen, workers, and soldiers, and together they represent an immense amount of animal biomass. These cockroaches are termites (Isoptera), an extremely ecologically successful group of predominantly tropical insects. Termites mostly feed on plant matter — especially on dead wood, though some species also feed on grass or soil. All of these food sources are virtually ubiquitous, but also hard to digest and poor in some essential nutrients, such as fatty acids. Termites owe their ecological success partly to their ability to utilise these dietary resources which remain inaccessible to most animals. A team of researchers led by Robert Hanus now furthered our knowledge of how this ability came to be. They focused on linoleic acid, a crucial nutrient that the ancestors of termites needed to synthesise de novo before switching to their current linoleic acid-poor diet.

Unsaturated fatty acids. Oleic acid (top) with a single double bond in position 9 and linoleic acid (bottom) with two double bonds in positions 9 and 12.
(Public domain)

Linoleic acid is a polyunsaturated fatty acid (PUFA), i.e., an unsaturated fatty acid containing two or more double bonds. Animals are usually unable to synthesise PUFAs and need to acquire them from their diet — in other words, PUFAs are essential nutrients. Notably, PUFAs are crucial precursors for the synthesis of cell membrane components, signal molecules (e.g., eicosanoids), or energy-storing triacylglycerols. Furthermore, insect cuticular hydrocarbons that protect the animal from desiccation or play a role in communication (nestmate recognition, etc.) are also derived from PUFAs, and the same can be said about some insect pheromones. The evolution of de novo linoleic acid biosynthesis is known from approximately 20 insect species from various lineages where this trait independently and repeatedly arose or was lost.

As has been stated above, termites are a group of cockroaches (Blattodea), with woodroaches (genus Cryptocercus) as a sister lineage to termites. Cryptocercus roaches also feed on wood and display parental care. All termites, Cryptocercus, and a few other lineages of cockroaches together constitute Blattoidea, a clade where de novo linoleic acid biosynthesis has been already described. Did the ability of linoleic acid biosynthesis evolve once in Blattoidea, and termites thus simply inherited it? Is this trait’s evolution more complex? To test the former hypothesis, the authors analysed sequence data from 57 species of termites and cockroaches. They focused on fatty acyl desaturases (FADs), enzymes responsible for the introduction of double bonds into fatty acids, i.e., synthesis of unsaturated fatty acids.

            The majority of analysed Δ12 FAD desaturases — responsible for the formation of linoleic acid — from various insect taxa share amino acid sequence similarities and sometimes even enzyme activity with Δ9 FADs producing oleic or palmitoleic acid. Δ12 FAD likely arose through a Δ9 FAD gene duplication. One of the paralogs then acquired a new function: enzyme activity allowing the introduction of a double bond in position 12. The authors identified this gene duplication in Blattoidea and tested the function of both gene products (with assumed Δ9 FAD or Δ12 FAD activity) by expressing them in desaturase-deficient yeast. In accordance with the hypothesis of the Δ12 FAD originating from gene duplication, the ancestral gene product displayed Δ9 FAD activity, while the product of the derived gene showed Δ12 FAD activity, i.e., conversion of oleic acid into linoleic acid. Site-directed mutagenesis and AlphaFold2-predicted protein 3D models allowed the authors to further correlate FAD structural details with particular enzyme activity and specificity.

A soldier individual of Prorhinotermes simplex, one of the analysed termite species with a molecular structure of Δ12 FAD from the same species (PsimFAD-A1b) as predicted by AlphaFold2 shown in the background. The depicted structure includes the substrate-binding portion of the active site.
Source: K. Bezányiová, based on a photograph by J. Šobotník and structural models from the original paper

            Thus, the authors conclude, the blattoidean ability to synthesise linoleic acid evolved only once roughly 160 Mya through a Δ9 FAD gene duplication followed by a subsequent neofunctionalisation of one of the paralogs. Unlike FADs in other insect lineages, the blattoidean Δ12 FAD remained conserved throughout 140 million years of termite evolution. The extant 3,000 termite species or so owe a part of their ecological success to this gene duplication. The resultant Δ12 FAD allowed the omnivorous cockroach ancestors of termites to specialise on food sources that could not cover the termites’ dietary needs. The dataset of FAD sequences from various insect lineages as well as FAD structural data compiled for the present study should aid the discovery of desaturases responsible for synthesis of dodecatrienol (Z3,Z6,E8-dodecatrienol), the most common termite pheromone, the molecule of which contains three double bonds. No other animal besides termites is known to produce this compound.

Macháček, S., Tupec, M., Horáček, N., Halmová, M., Roy, A., Machara, A., Kyjaková, P., Lukšan, O., Pichová, I., & Hanus, R. (2023). Evolution of Linoleic Acid Biosynthesis Paved the Way for Ecological Success of Termites. Molecular Biology and Evolution, 40(4), msad087.

Kateřina Bezányiová