PDF(Pubmed)
Abstract：
Macrotermitine termites have domesticated fungi in the genus Termitomyces as their primary food source using predigested plant biomass. To access the full nutritional value of lignin-enriched plant biomass, the termite-fungus symbiosis requires the depolymerization of this complex phenolic polymer. While most previous work suggests that lignocellulose degradation is accomplished predominantly by the fungal cultivar, our current understanding of the underlying biomolecular mechanisms remains rudimentary. Here, we provide conclusive omics and activity-based evidence that Termitomyces employs not only a broad array of carbohydrate-active enzymes (CAZymes) but also a restricted set of oxidizing enzymes (manganese peroxidase, dye decolorization peroxidase, an unspecific peroxygenase, laccases, and aryl-alcohol oxidases) and Fenton chemistry for biomass degradation. We propose for the first time that Termitomyces induces hydroquinone-mediated Fenton chemistry (Fe2+ + H2O2 + H+ → Fe3+ + •OH + H2O) using a herein newly described 2-methoxy-1,4-dihydroxybenzene (2-MH2Q, compound 19)-based electron shuttle system to complement the enzymatic degradation pathways. This study provides a comprehensive depiction of how efficient biomass degradation by means of this ancient insect\'s agricultural symbiosis is accomplished. IMPORTANCE Fungus-growing termites have optimized the decomposition of recalcitrant plant biomass to access valuable nutrients by engaging in a tripartite symbiosis with complementary contributions from a fungal mutualist and a codiversified gut microbiome. This complex symbiotic interplay makes them one of the most successful and important decomposers for carbon cycling in Old World ecosystems. To date, most research has focused on the enzymatic contributions of microbial partners to carbohydrate decomposition. Here, we provide genomic, transcriptomic, and enzymatic evidence that Termitomyces also employs redox mechanisms, including diverse ligninolytic enzymes and a Fenton chemistry-based hydroquinone-catalyzed lignin degradation mechanism, to break down lignin-rich plant material. Insights into these efficient decomposition mechanisms reveal new sources of efficient ligninolytic agents applicable for energy generation from renewable sources.
摘要：
大白蚁利用预消化的植物生物质将白蚁属中的真菌驯化为其主要食物来源。为了获得富含木质素的植物生物质的全部营养价值，白蚁-真菌共生需要这种复杂的酚类聚合物的解聚。虽然大多数以前的工作表明，木质纤维素降解主要是由真菌品种完成的，我们目前对潜在的生物分子机制的理解仍然是基本的。这里,我们提供了结论性的组学和基于活性的证据，表明Termitomyces不仅采用了广泛的碳水化合物活性酶（CAZymes），而且还采用了一组有限的氧化酶（锰过氧化物酶，染料脱色过氧化物酶，一种非特异性的过氧化酶,漆酶,和芳基醇氧化酶）和Fenton化学用于生物质降解。我们首次提出使用本文新描述的2-甲氧基-1,4-二羟基苯（2-MH2Q，化合物19）为基础的电子穿梭系统，以补充酶促降解途径。这项研究全面描述了如何通过这种古老的昆虫的农业共生来实现有效的生物质降解。重要性真菌生长的白蚁通过参与三方共生以及真菌互助者和共同多样化的肠道微生物组的互补贡献，优化了顽固植物生物质的分解，以获取有价值的养分。这种复杂的共生相互作用使它们成为旧世界生态系统中碳循环最成功和最重要的分解者之一。迄今为止,大多数研究集中在微生物伴侣对碳水化合物分解的酶作用上。这里,我们提供基因组，转录组，和酶的证据表明，白蚁菌也有氧化还原机制，包括多种木质素分解酶和基于Fenton化学的对苯二酚催化木质素降解机理，分解富含木质素的植物材料。对这些有效分解机制的见解揭示了适用于可再生能源产生的有效木质素分解剂的新来源。
