Termite-engineered microbial communities of termite nest structures: a new dimension to the extended phenotype

Abstract

Termites are a prototypical example of the 'extended phenotype' given their ability to shape their environments by constructing complex nesting structures and cultivating fungus gardens. Such engineered structures provide termites with stable, protected habitats, and nutritious food sources, respectively. Recent studies have suggested that these termite-engineered structures harbour Actinobacteria-dominated microbial communities. In this review, we describe the composition, activities, and consequences of microbial communities associated with termite mounds, other nests, and fungus gardens. Culture-dependent and culture-independent studies indicate that these structures each harbour specialized microbial communities distinct from those in termite guts and surrounding soils. Termites select microbial communities in these structures through various means: opportunistic recruitment from surrounding soils; controlling physicochemical properties of nesting structures; excreting hydrogen, methane, and other gases as bacterial energy sources; and pretreating lignocellulose to facilitate fungal cultivation in gardens. These engineered communities potentially benefit termites by producing antimicrobial compounds, facilitating lignocellulose digestion, and enhancing energetic efficiency of the termite 'metaorganism'. Moreover, mound-associated communities have been shown to be globally significant in controlling emissions of methane and enhancing agricultural fertility. Altogether, these considerations suggest that the microbiomes selected by some animals extend much beyond their bodies, providing a new dimension to the 'extended phenotype'.

Keywords: Actinobacteria; animal–microbe interactions; ecosystem engineering; methane; symbiosis.

Figure 1.

Photographs demonstrating the importance of termite mounds in tropical regions. (A) As ecologically dominant eusocial organisms, millions of enormous soil mounds constructed by Syntermes termites span 230 000 km² of Northeast Brazil and persist for up to 4000 years (Martin et al. 2018). (B) Extensive termite mounds in a dry grassy field in Brazil.

Figure 2.

Photographs and tomographs of the complex internal structures and external morphologies of nesting structures across termite species. The external and internal structures of three north Australian termite species are shown, namely the wood-feeding Microcerotermes nervosus (A) and (B), soil-interface feeding Macrognathotermes sunteri (C) and (D), and grass-feeding Tumulitermes pastinator (E) and (F) are shown. The cross-section binary images are based on X-ray computer tomography (CT scanning; Nauer et al. 2018a). Also shown are the subterranean nests (G) and fungal garden (H) of the fungus-farming species Odontermes formosanus (Li et al. 2017).

Figure 3.

Overview of the microbial mediators of key biogeochemical processes in termite guts and mounds. The diagram shows how termite gut microbial processes results in the conversion of lignocellulose and other organic matter into the gases carbon dioxide (CO₂), hydrogen (H₂), and methane (CH₄). Mound-associated bacteria consume these gases as energy and carbon sources, though there are still significant emissions of the greenhouse gases carbon dioxide and methane into the atmosphere. The key microbial phyla that mediate the consumption and production of these gases, as well as lignocellulose degradation, are also shown.

Figure 4.

Composition and metabolic capabilities of the microbial communities of termite mounds and surrounding soils. (A) Relative abundance of microbial phyla based on read mapping of metagenomes using GraftM. (B) Percentage of microbial communities that mediate different metabolic processes. Results are shown for three different termite species, namely the wood-feeding Microcerotermes nervosus, soil-interface feeding Macrognathotermes sunteri, grass-feeding Tumulitermes pastinator, as previously described (Chiri et al. 2021).