Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, OK, USA.
Department of Biological Sciences, University of Toronto Scarborough, Toronto, ON, Canada.
Nat Commun. 2024 Mar 28;15(1):2714. doi: 10.1038/s41467-024-47047-4.
Anaerobic gut fungi (AGF, Neocallimastigomycota) reside in the alimentary tract of herbivores. While their presence in mammals is well documented, evidence for their occurrence in non-mammalian hosts is currently sparse. Culture-independent surveys of AGF in tortoises identified a unique community, with three novel deep-branching genera representing >90% of sequences in most samples. Representatives of all genera were successfully isolated under strict anaerobic conditions. Transcriptomics-enabled phylogenomic and molecular dating analyses indicated an ancient, deep-branching position in the AGF tree for these genera, with an evolutionary divergence time estimate of 104-112 million years ago (Mya). Such estimates push the establishment of animal-Neocallimastigomycota symbiosis from the late to the early Cretaceous. Further, tortoise-associated isolates (T-AGF) exhibited limited capacity for plant polysaccharides metabolism and lacked genes encoding several carbohydrate-active enzyme (CAZyme) families. Finally, we demonstrate that the observed curtailed degradation capacities and reduced CAZyme repertoire is driven by the paucity of horizontal gene transfer (HGT) in T-AGF genomes, compared to their mammalian counterparts. This reduced capacity was reflected in an altered cellulosomal production capacity in T-AGF. Our findings provide insights into the phylogenetic diversity, ecological distribution, evolutionary history, evolution of fungal-host nutritional symbiosis, and dynamics of genes acquisition in Neocallimastigomycota.
厌氧肠道真菌（AGF，Neocallimastigomycota）存在于草食动物的消化道中。虽然它们在哺乳动物中的存在已被充分记录，但目前关于它们在非哺乳动物宿主中存在的证据还很稀少。对乌龟中 AGF 的非培养调查确定了一个独特的群落，其中三个新的深分枝属代表了大多数样本中超过 90%的序列。所有属的代表都在严格的厌氧条件下成功分离。基于转录组学的系统发育基因组学和分子定年分析表明，这些属在 AGF 树中具有古老的、深分枝的位置，其进化分歧时间估计为 1.04-1.12 亿年前（Mya）。这些估计将动物-Neocallimastigomycota 共生的建立时间从晚白垩世推至早白垩世。此外，与乌龟相关的分离物（T-AGF）表现出有限的植物多糖代谢能力，并且缺乏编码几种碳水化合物活性酶（CAZyme）家族的基因。最后，我们证明，与哺乳动物相比，T-AGF 基因组中水平基因转移（HGT）的缺乏导致了观察到的降解能力受限和 CAZyme 库减少，这反映在 T-AGF 中改变的纤维小体产生能力上。我们的研究结果为 Neocallimastigomycota 的系统发育多样性、生态分布、进化历史、真菌-宿主营养共生的进化以及基因获取的动态提供了深入的见解。
