The digestive system in Zygentoma as a model for high cellulase activity

Authors: POTHULA, RATNASRI - University Of Tennessee; SHIRLEY, DEREK - University Of Tennessee; Perera, Omaththage; KLINGEMAN, WILLIAM - University Of Tennessee; OPPERT, CRIS - University Of Tennessee; ABD-ELGAFFAR, HEBA M.Y. - University Of Tennessee; JOHNSON, BRIAN - University Of California, Davis; JURAT-FUENTES, JUAN LUIS - University Of Tennessee

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2019
Publication Date: 2/28/2019
Citation: Pothula, R., Shirley, D., Perera, O.P., Klingeman, W.E., Oppert, C., Abd-Elgaffar, H., Johnson, B.R., Jurat-Fuentes, J. 2019. The digestive system in Zygentoma as a model for high cellulase activity. PLoS One. 14(2):e0212505.

Interpretive Summary: Firebrats and silverfish (order Zygentoma) are capable of digesting cellulose containing material such as paper and cotton fibers. Activities of cellulose digesting enzymes in the gray silverfish (Ctenolepisma longicaudata) and firebrat (Thermobia domestica) were characterized using quantitative and qualitative cellulase assays, proteomics, transcriptomics, and morphohistological studies. Enzyme assays identified the foregut as the region with the highest levels of cellulolytic activity in both firebrat and gray silverfish. Putative beta 1,4-endoglucanases matching insect or arthropod enzymes and glucan endo-1,6-beta-glucosidases matching bacterial enzymes were identified in this study. These findings support combined activities of endogenous and symbiont-derived plant cell wall degrading enzymes in lignocellulose digestion in Zygentoma and advance the identification of novel cellulolytic system with potential application in the biofuel industry.

Technical Abstract: The digestive system of selected phytophagous insects has been examined as a potential prospecting resource for novel cellulolytic enzymes with industrial applications. In contrast to other model species, however, limited detailed information is available that characterizes cellulolytic activity and systems in basal hexapods. As part of a screening effort to identify insects with highly active cellulolytic systems, we identified species of Zygentoma that displayed the highest cellulolytic activity compared to known model species for cellulolytic systems such as Termitoidea (formerly Isoptera) or Blattidae (formerly Blattaria). The goal of the present study was to provide a morphohistological characterization of cellulose digestion and to identify highly active cellulase enzymes present in digestive fluids of Zygentoma species. Morphohistological characterization supported no relevant differences in the digestive system of firebrat (Thermobia domestica (Packard)) and the gray silverfish (Ctenolepisma longicaudata Escherich). Quantitative and qualitative cellulase assays identified the foregut as the region with the highest levels of cellulolytic activity in both T. domestica and C. longicaudata. However, T. domestica was found to have higher endoglucanase, xylanase and pectinase activities compared to C. longicaudata. Using nano liquid chromatography coupled to tandem mass spectrometry (nanoLC/MS/MS) and a custom gut transcriptome we identified cellulolytic enzymes from digestive fluids of T. domestica. Among the identified enzymes we report putative beta 1,4-endoglucanases matching to arthropod enzymes and bacterial glucan endo-1,6-beta-glucosidases. These findings support combined activities of endogenous and symbiont-derived plant cell wall degrading enzymes in lignocellulose digestion in Zygentoma and advance the identification of novel cellulolytic system with potential application in the biofuel industry.