The relationship between oxidant levels and gut physiology in a litter-feeding termite

Abstract

The termite gut is an efficient decomposer of polyphenol-rich diets, such as lignocellulosic biomasses, and it has been proposed that non-enzymatic oxidative mechanisms could be involved with the digestive process in these animals. However, oxidant levels are completely unknown in termites, as well as protective mechanisms against oxidative damage to the termite gut and its microbiota. As the first step in investigating the role oxidants plays in termite gut physiology, this work presents oxidant levels, antioxidant enzymatic defenses, cell renewal and microbiota abundance along the litter-feeding termite Cornitermes cumulans gut compartments (foregut, midgut, mixed segment and hindgut p1, p3, p4, and p5 segments) and salivary glands. The results show variable levels of oxidants along the C. cumulans gut, the production of antioxidant enzymes, gut cell renewal as potential defenses against oxidative injuries and the profile of microbiota distribution (being predominantly inverse to oxidant levels). In this fashion, the oxidative challenges imposed by polyphenol-rich diet seem to be circumvented by the C. cumulans gut, ensuring efficiency of the digestive process together with preservation of tissue homoeostasis and microbiota growth. These results present new insights into the physicochemical properties of the gut in a litter-feeding termite, expanding our view in relation to termites’ digestive physiology.

Symbiont coordinates stem cell proliferation, apoptosis, and morphogenesis of gut symbiotic organ in the stinkbug-Caballeronia symbiosis

“…Besides the suppression of apoptosis in the tip part of crypts, the gut-colonizing Caballeronia symbiont simultaneously induces cell divisions of ISCs at the crypt base, revealed mostly by the enhanced signal from the EdU marker of DNA replication. PH3 on the other hand is a well-known marker of mitosis ( Hirota et al, 2005 ; Lin et al, 2008 ; Buchon et al, 2009 ) and immunostaining of PH3 has been widely used in numerous insect species including Drosophila , termites and planthoppers to reveal mitotic cells ( Buchon et al, 2009 ; Sousa et al, 2019 ; Guo et al, 2020 ). In this study, we performed the immunostaining of PH3 to reveal the localization of mitotic cells in midgut crypts.…”

Oxidative cleavage of polysaccharides by a termite-derived superoxide dismutase boosts the degradation of biomass by glycoside hydrolases

“…This phenomenon is similar to that reported in the wood-feeding lower termites R. flavipes , 63 and Coptotermes formosanus 64 as well as for the litter-feeding Cornitermes cumulans , which also exhibit high levels of ROS in the fore- and mid-guts, allied with a high abundance of mRNA for Cc SD (Cu/Zn SOD) and glutathione peroxidase ( Cc GPX). 65–67…”

“…This phenomenon is similar to that reported in the wood-feeding lower termites R. flavipes, 63 and Coptotermes formosanus 64 as well as for the litter-feeding Cornitermes cumulans, which also exhibit high levels of ROS in the fore-and mid-guts, allied with a high abundance of mRNA for CcSD (Cu/Zn SOD) and glutathione peroxidase (CcGPX). [65][66][67] CgSOD-1 mediates an oxidative mechanism for the degradation of glucose polymers akin to that of the product profile exhibited by fungal and bacterial LPMOs 5,6,68,69 and likewise acts in synergy with classical glycoside hydrolases. Notably, activity on β-glucan and CMC reported here is specific for CgSOD-1, no effects were observed for BtSOD-1, one of the most studied vertebrate Cu/Zn SODs.…”

“…For the last two decades, scientists have reported that detritivore insect guts, such as caterpillars, beetles, and termites, produce considerable amounts of reactive oxygen species (ROS) involved in the degradation of plant-derived phenolic compounds and tannins. 13,65,66 Recent studies have hypothesized that this ROS generation could enhance plant cell wall degradation by boosting the activity of endogenous cellulases. 19,27,31 It is in this regard that the role Cu/Zn SODs discovered in our report now solves a long-running puzzle of how detritivore insect guts produce ROS in their guts and why endogenous termite hydrolases do not exhibit high catalytic performance on insoluble and recalcitrant polysaccharides.…”

Microbial Response to Fungal Infection in a Fungus-Growing Termite, Odontotermes formosanus (Shiraki)

“…The physiological environment of the gut is also correlated with microbial abundance. In the hindgut, oxide levels are inversely related to microbiota abundance ( Sousa et al, 2019 ), which could also indicate that an anaerobic hindgut environment created by high hindgut microbiota abundance is not conducive to the growth of Metarhizium . Moreover, the hindgut is located close to the rectum and the feces are also antimicrobially active, although the source of this antimicrobial activity is not known.…”