Department of Animal and Range Sciences, Montana State University, Bozeman, Montana, USA.
Biotechnology Center, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA.
mBio. 2021 Mar 3;12(2):e03533-20. doi: 10.1128/mBio.03533-20.
, , and are the three predominant cellulolytic bacterial species found in the rumen. studies have shown that these species compete for adherence to, and growth upon, cellulosic biomass. Yet their molecular interactions have not heretofore been examined. Gnotobiotically raised lambs harboring a 17-h-old immature microbiota devoid of culturable cellulolytic bacteria and methanogens were inoculated first with S85 and sp. strain 87.7, and 5 months later, the lambs were inoculated with 8 and FD-1. Longitudinal samples were collected and profiled for population dynamics, gene expression, fibrolytic enzyme activity, fibrolysis, and metabolite profiling. Quantitative PCR, metagenome and metatranscriptome data show that establishes at high levels initially but is gradually outcompeted following the introduction of the ruminococci. This shift resulted in an increase in carboxymethyl cellulase (CMCase) and xylanase activities but not in greater fibrolysis, suggesting that and ruminococci deploy different but equally effective means to degrade plant cell walls. Expression profiles showed that relied upon outer membrane vesicles and a diverse repertoire of CAZymes, while and preferred type IV pili and either CBM37-harboring or cellulosomal carbohydrate-active enzymes (CAZymes), respectively. The changes in cellulolytics also affected the rumen metabolome, including an increase in acetate and butyrate at the expense of propionate. In conclusion, this study provides the first demonstration of competition between the three predominant cellulolytic bacteria and provides insight on the influence of these ecological interactions on rumen fibrolytic function and metabolomic response. Ruminant animals, including cattle and sheep, depend on their rumen microbiota to digest plant biomass and convert it into absorbable energy. Considering that the extent of meat and milk production depends on the efficiency of the microbiota to deconstruct plant cell walls, the functionality of predominant rumen cellulolytic bacteria, , , and , has been extensively studied to obtain a better knowledge of how they operate to hydrolyze polysaccharides and ultimately find ways to enhance animal production. This study provides the first evidence of competitions between and the two species. It shows that a simple disequilibrium within the cellulolytic community has repercussions on the rumen metabolome and fermentation end products. This finding will have to be considered in the future when determining strategies aiming at directing rumen fermentations for animal production.
、 和 是瘤胃中三种主要的纤维分解细菌。研究表明，这些物种竞争对纤维素生物质的附着和生长。然而，它们的分子相互作用迄今尚未被研究。无菌饲养的羔羊，其 17 小时龄的不成熟微生物群中缺乏可培养的纤维分解细菌和产甲烷菌，首先用 S85 和 种 87.7 接种，5 个月后，羔羊用 8 和 FD-1 接种。纵向样本被收集并对种群动态、基因表达、纤维分解酶活性、纤维分解和代谢物谱进行分析。定量 PCR、宏基因组和宏转录组数据表明， 最初高水平定植，但在引入瘤胃球菌后逐渐被淘汰。这种转变导致羧甲基纤维素酶 (CMCase) 和木聚糖酶活性增加，但纤维分解作用没有增加，这表明 和瘤胃球菌使用不同但同样有效的方法来降解植物细胞壁。表达谱显示， 依赖于外膜囊泡和多种 CAZymes，而 和 分别更喜欢 IV 型菌毛和含有 CBM37 的或纤维素酶碳水化合物活性酶 (CAZymes)。纤维分解物的变化也影响了瘤胃代谢组，包括以丙酸为代价增加乙酸和丁酸。总之，本研究首次证明了三种主要纤维分解细菌之间的 竞争，并提供了对这些生态相互作用如何影响瘤胃纤维分解功能和代谢组学反应的见解。反刍动物，包括牛和羊，依赖于它们的瘤胃微生物群来消化植物生物质并将其转化为可吸收的能量。考虑到肉类和牛奶产量的程度取决于微生物群分解植物细胞壁的效率，主要瘤胃纤维分解细菌 、 、 和 的功能已经得到了广泛的研究，以更好地了解它们如何水解多糖并最终找到提高动物生产的方法。本研究首次提供了 与两种 物种之间竞争的证据。它表明，纤维分解菌群落中的简单失衡会对瘤胃代谢组和发酵终产物产生影响。在未来确定旨在指导动物生产的瘤胃发酵策略时，需要考虑到这一发现。
