Lignocellulose Decomposition In A Fungus-Growing Termite,Odontotermes Formosanus Shiraki(Blattodea:Termitidae,Macrotermitinae)

Termites(Blattodea: Termitidae)are eusocial arthropod decomposers,and improve soil fertility,crop yield,and also are used by humans for their benefits across the world.However,the fungus-growing termites(subfamily Macrotermitinae)are the most successful and highly efficient in degrading and digesting plant biomass.They have a mutualist association with fungi of the genus Termitomyces(Basidiomycota,Agaricales,Lyophyllaceae)and gut microbiota to support the near-complete decomposition of lignocellulose to gain access to nutrients.This elaborate strategy of plant biomass digestion makes them ecologically successful dominant decomposers in(sub)-tropical Old World ecosystems.However,the process of lignocellulose degradation in these termites is poorly understood.Insights into where specific plant biomass components are targeted during the decomposition process are also sparse.In the present study,several analytical approaches were performed on the fate of plant biomass components to examine which lignocellulose components digested throughout the decomposition process in a fungus-growing termite,Odontotermes formosanus(Shiraki).The results revealed physical disruption of the lignocellulose structure in termite guts and fungus combs,which was consistent with the degradation capabilities of fresh,mature,and old fungus combs for cellulose,hemicellulose,and lignin.This study showed a gradual reduction of lignin,cellulose,and hemicellulose from 256.6±9.2,513.3±8.2,and 152.5±2.5 mg/g in mulberry wood to 208.2±4.4,456.5±8.6,and 129.6±1.9 mg/g in fresh comb;110.6±1.9,303.0±7.4,and 102.9±1.2 mg/g in mature comb,and 94.9±2.1,176.9±5.9,and 71.0±1.5 mg/g in old comb,respectively.Our results showed that the crystallinity index(%)was also significantly reduced in fresh(36.1±0.8%),mature(31.9±0.6%),and old comb(25.0±0.6%)compared to mulberry(38.5±1.3%).Significant changes in guaiacyl,syringyl and phydroxyphenyl lignin units were recorded in fresh(56.8±8.5,41.8±6.5,and 10.6±1.8 μg),mature(22.2±2.4,15.9±1.5,and 3.8±0.8 μg)and old comb(19.0±0.6,14.1±0.1,and 4.1±0.7μg)compared to original wood(92.4±6.7,46.2±3.4,and 7.2±0.1 μg,respectively).Furthermore,the high diversity of monomeric sugars(particularly glucose,xylose,arabinose,ribose,galacturonic acid,and N-acetylglucosamine)was recorded in mature comb samples.Our findings support that the young workers initiates the degradation of lignocellulose but leaves most of the lignin,hemicellulose,and cellulose in fresh comb,where decomposition primarily occurs.A gradual reduction of plant polymers across different stages of decomposition was observed.The results revealed that young workers and fungus comb efficiently degrade the lignocellulose resulting the old comb enriched with simple sugars.The well decomposed old comb is ingested by old workers,where the final decomposition occurs.Amplicon sequencing of 16 S r RNA gene was also applied to investigate which bacteria are abundant across different stages in the degradation process.Our results provided new insights in bacterial composition in the symbiotic system of O.formosanus.The most dominant bacterial taxa were Alistipes(0.15±0.06% to 28.53±2.84%),Bradyrhizobium(0.00±0.00% to 22.17±10.49%),Parabacteroides(0.11±0.04% to 9.43±1.77%),and Dysgonomonas(0.02±0.01% to 10.47±0.64%)throughout the digestion process.However,distinct bacterial communities were associated with different stages of decomposition.The higher relative abundances of Candidatus＿Tammella in young workers,Dysgonomonas and Treponema in fresh comb,Candidatus＿Udaeobacter in mature comb,Bradyrhizobium and Mycobacterium in old comb,and Breznakia in old workers were the most obvious difference observed.The unique bacterial lineages at different sites of degradation could work synergistically with Termitomyces fungus and potentially contribute to the breakdown of particular plant components.Our findings indicate that the gut microbial communities of young workers utilize non-cellulosic polysaccharides and provide nutrition to the host.The fresh comb bacteria work synergistically with Termitomyces to boost the degradation of lignocellulose components.The lignocellulolytic activity within the fresh comb reduces the amount of lignocellulose and increases the carbohydrates in older combs,where some dominant bacterial taxa may work collaboratively with fungus to degrade carbohydrates.The gut microbiota of old workers preferentially uses simple sugars and provide nutrition to the host.