Abstract
The survival and foraging of Coptotermes formosanus Shiraki in a microbe-rich environment reflect the adaptation of an extraordinary, sophisticated defense mechanism by the nest-mates. We aimed to explore the host pathogen interaction by studying caste-specific volatile chemistry and genes encoding the antioxidant defense of winged imagoes, nymphs, soldiers and workers of Formosan subterranean termites. Qualitative analyses of C. formosanus Shiraki performed by HS-SPME/GC-MS showed considerable variations in the chemical composition of volatile organic compounds (VOCs) and their proportions among all the castes. Winged imagoes produced the most important compounds such as naphthalene and n-hexanoic acid. The antifungal activity of these compounds along with nonanal, n-pentadecane, n-tetradecane, n-heptadecane and methyl octanoate against the conidial suspensions of Metarhizium anisopliae and Beauveria bassiana isolates enable us to suggest that the failure of natural fungal infection in the nest is due to the antiseptic environment of the nest, which is mainly controlled by the VOCs of nest-mates. In addition, conidial germination of M. anisopliae and B. bassiana isolates evaluated on the cuticle of each caste showed significant variations among isolates and different castes. Our results showed that the conidia of M. anisopliae 02049 exhibited the highest germination on the cuticle of all the inoculated castes. Moreover, we recorded the lowest germination of the conidia of B. bassiana 200436. Caste-specific germination variations enabled us to report for the first time that the cuticle of winged imagoes was found to be the most resistant cuticle. The analysis of the transcriptome of C. formosanus Shiraki revealed the identification of 17 genes directly involved in antioxidant defense. Expression patterns of the identified antioxidant genes by quantitative real-time PCR (qPCR) revealed the significantly highest upregulation of CAT, GST, PRXSL, Cu/Zn-SOD2, TXN1, TXN2, TXNL1, TXNL2, TXNL4A and TPx genes among winged imagoes upon infection with the most virulent isolate, M. anisopliae 02049. Furthermore, soldiers showed the least expression of genes encoding antioxidant defense. Our findings indicated that the volatile chemistry of nest-mates and genes encoding antioxidant defense greatly contribute to the survival and foraging of Formosan subterranean termites in a microbe-rich habitat.
Highlights
Formosan subterranean termites, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), a possible threat to the economies of the world, live in complex networks of galleries or tunnels below the soil surface or encased in wood in close social groups consisting of millions of individuals jammed together within the nest
HS-SPME analyses of the volatiles have revealed an impressive diversity of chemical components in C. formosanus Shiraki: fatty acids, aldehydes, aromatics, heterocyclic aromatics, flavanoids, sesquiterpenes, straight-chained and branched alkanes, ketones, esters, alcohols and nitrogen- or sulfur-containing compounds (Table 1)
The identification and origin of important compounds from volatile organic compounds (VOCs) of colony members with proven antifungal activity and mining the genes encoding the antioxidant defense of C. formosanus Shiraki and their expression patterns against fungal infections revealed in the current study profoundly widen the knowledge on disease resistance in termites in addition to previously explored social behavioral disease resistance interactions [4,5,20,21] and the immune mechanisms of disease resistance [7]
Summary
Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), a possible threat to the economies of the world, live in complex networks of galleries or tunnels below the soil surface or encased in wood in close social groups consisting of millions of individuals jammed together within the nest. Termites are considered ecologically important because they facilitate the cellulose degradation that recycles the nutrients back into the soil [1]. Their beneficial role as a decomposer changes to “pest” when they encounter commodities important for human consumption including forest and agronomic vegetation used for construction and human consumption, respectively. The huge economic losses caused by the termites all around the world have over-shadowed their beneficial role as decomposers. Concerns over human health and environmental pollution by liquid termiticides and the limitations of both the non-repellant and repellent termiticides have provided the impetus to look for alternative methods to control termites
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