RG Insect Microbiology and Symbiosis, Max Planck Institute for Terrestrial Microbiology, 35043, Marburg, Germany.
Tropical Biosphere Research Center, Center of Molecular Biosciences, University of the Ryukyus, Nishihara, Okinawa, 903-0213, Japan.
Microbiome. 2024 Oct 15;12(1):201. doi: 10.1186/s40168-024-01917-7.
The microbial landscape within termite guts varies across termite families. The gut microbiota of lower termites (LT) is dominated by cellulolytic flagellates that sequester wood particles in their digestive vacuoles, whereas in the flagellate-free higher termites (HT), cellulolytic activity has been attributed to fiber-associated bacteria. However, little is known about the role of individual lineages in fiber digestion, particularly in LT.
We investigated the lignocellulolytic potential of 2223 metagenome-assembled genomes (MAGs) recovered from the gut metagenomes of 51 termite species. In the flagellate-dependent LT, cellulolytic enzymes are restricted to MAGs of Bacteroidota (Dysgonomonadaceae, Tannerellaceae, Bacteroidaceae, Azobacteroidaceae) and Spirochaetota (Breznakiellaceae) and reflect a specialization on cellodextrins, whereas their hemicellulolytic arsenal features activities on xylans and diverse heteropolymers. By contrast, the MAGs derived from flagellate-free HT possess a comprehensive arsenal of exo- and endoglucanases that resembles that of termite gut flagellates, underlining that Fibrobacterota and Spirochaetota occupy the cellulolytic niche that became vacant after the loss of the flagellates. Furthermore, we detected directly or indirectly oxygen-dependent enzymes that oxidize cellulose or modify lignin in MAGs of Pseudomonadota (Burkholderiales, Pseudomonadales) and Actinomycetota (Actinomycetales, Mycobacteriales), representing lineages located at the hindgut wall.
The results of this study refine our concept of symbiotic digestion of lignocellulose in termite guts, emphasizing the differential roles of specific bacterial lineages in both flagellate-dependent and flagellate-independent breakdown of cellulose and hemicelluloses, as well as a so far unappreciated role of oxygen in the depolymerization of plant fiber and lignin in the microoxic periphery during gut passage in HT. Video Abstract.
白蚁肠道内的微生物景观因白蚁家族而异。低等白蚁（LT）的肠道微生物群主要由能够将木质颗粒隔离在其消化液泡中的纤维素鞭毛虫组成，而在没有鞭毛虫的高等白蚁（HT）中，纤维素的活性归因于纤维相关的细菌。然而，人们对个别谱系在纤维消化中的作用知之甚少，特别是在 LT 中。
我们调查了从 51 种白蚁肠道宏基因组中回收的 2223 个宏基因组组装基因组（MAG）的木质纤维素分解潜力。在依赖鞭毛虫的 LT 中，纤维素酶仅限于 Bacteroidota（Dysgonomonadaceae、Tannerellaceae、Bacteroidaceae、Azobacteroidaceae）和 Spirochaetota（Breznakiellaceae）的 MAG，反映了对纤维二糖的专门化，而它们的半纤维素酶库则具有对木聚糖和各种杂多糖的活性。相比之下，源自无鞭毛虫的 HT 的 MAG 具有全面的外切和内切葡聚糖酶 arsenal，类似于白蚁肠道鞭毛虫的 arsenal，这表明 Fibrobacterota 和 Spirochaetota 占据了鞭毛虫丢失后空缺的纤维素分解生态位。此外，我们在 Pseudomonadota（Burkholderiales、Pseudomonadales）和 Actinomycetota（Actinomycetales、Mycobacteriales）的 MAG 中检测到直接或间接依赖氧气的酶，这些酶氧化纤维素或修饰木质素，代表位于后肠壁的谱系。
本研究的结果细化了我们对白蚁肠道木质纤维素共生消化的概念，强调了特定细菌谱系在依赖鞭毛虫和不依赖鞭毛虫的纤维素和半纤维素分解中的不同作用，以及氧气在 HT 中肠道通过时微氧环境中植物纤维和木质素解聚的作用。
