Abstract
Lignocellulose digestion in termites is achieved through the functional synergy between gut symbionts and host enzymes. However, some species have evolved additional associations with nest microorganisms that collaborate in the decomposition of plant biomass. In a previous study, we determined that plant material packed with feces inside the nests of Cornitermes cumulans (Syntermitinae) harbors a distinct microbial assemblage. These food nodules also showed a high hemicellulolytic activity, possibly acting as an external place for complementary lignocellulose digestion. In this study, we used a combination of ITS sequence analysis, metagenomics, and metatranscriptomics to investigate the presence and differential expression of genes coding for carbohydrate-active enzymes (CAZy) in the food nodules and the gut of workers and soldiers. Our results confirm that food nodules express a distinct set of CAZy genes suggesting that stored plant material is initially decomposed by enzymes that target the lignin and complex polysaccharides from fungi and bacteria before the passage through the gut, where it is further targeted by a complementary set of cellulases, xylanases, and esterases produced by the gut microbiota and the termite host. We also showed that the expression of CAZy transcripts associated to endoglucanases and xylanases was higher in the gut of termites than in the food nodules. An additional finding in this study was the presence of fungi in the termite gut that expressed CAZy genes. This study highlights the importance of externalization of digestion by nest microbes and provides new evidence of complementary digestion in the context of higher termite evolution.
Highlights
Termites (Blattodea: Isoptera) are eusocial cockroaches comprising over 3,000 species widespread in tropical and subtropical regions
Termites rely on a mutualistic association with gut symbionts to decompose the plant biomass; the digestive efficiency is achieved by the functional complementation with host endogenous lignocellulases (Tokuda and Watanabe, 2007; Scharf, 2008; Scharf et al, 2011)
We present evidences of complementary digestion by external nest microorganisms in a neotropical grassharvester termite C. cumulans (Syntermitinae) that store plant material inside its nests (Figure 3F)
Summary
Termites (Blattodea: Isoptera) are eusocial cockroaches comprising over 3,000 species widespread in tropical and subtropical regions. These insects play an important role in ecosystems through the decomposition of plant lignocellulose (Brune, 2014; Mikaelyan et al, 2015), having a positive impact in nutrient cycling and soil-water dynamics through the construction of their nests and tunnel networks in soil (Neupane et al, 2015; Siebers et al, 2015; Jouquet et al, 2018). Higher termites (Termitidae) have evolved remarkable nesting strategies including the construction of epigeal mounds which can reach a prominent size in some species (Korb, 2011). Some authors have hypothesized that externalization of digestion by nest microorganisms, as seen in the subfamilies Macrotermitinae and Sphaerotermitinae (Garnier-Sillam et al, 1989; Aanen et al, 2002), was the first step in the evolution of Termitidae and might have driven the loss of gut protozoans and the acquisition of specialized lignocellulolytic bacteria resulting in higher efficiency in plant decomposition (Brune, 2014; Chouvenc et al, 2021)
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