Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities

Nikola Palevich; William J. Kelly; Sinead C. Leahy; Stuart Denman; Eric Altermann; Jasna Rakonjac; Graeme T. Attwood

摘要

Plant polysaccharide breakdown by microbes in the rumen is fundamental to digestion in ruminant livestock. Bacterial species belonging to the rumen genera Butyrivibrio and Pseudobutyrivibrio are important degraders and utilizers of lignocellulosic plant material. These bacteria degrade polysaccharides and ferment the released monosaccharides to yield short-chain fatty acids that are used by the ruminant for growth and the production of meat, milk, and fiber products. Although rumen Butyrivibrio and Pseudobutyrivibrio species are regarded as common rumen inhabitants, their polysaccharide-degrading and carbohydrate-utilizing enzymes are not well understood. In this study, we analyzed the genomes of 40 Butyrivibrio and 6 Pseudobutyrivibrio strains isolated from the plant-adherent fraction of New Zealand dairy cows to explore the polysaccharide-degrading potential of these important rumen bacteria. Comparative genome analyses combined with phylogenetic analysis of their 16S rRNA genes and short-chain fatty acid production patterns provide insight into the genomic diversity and physiology of these bacteria and divide Butyrivibrio into 3 species clusters. Rumen Butyrivibrio bacteria were found to encode a large and diverse spectrum of degradative carbohydrate-active enzymes (CAZymes) and binding proteins. In total, 4,421 glycoside hydrolases (GHs), 1,283 carbohydrate esterases (CEs), 110 polysaccharide lyases (PLs), 3,605 glycosyltransferases (GTs), and 1,706 carbohydrate-binding protein modules (CBM) with predicted activities involved in the depolymerization and transport of the insoluble plant polysaccharides were identified. Butyrivibrio genomes had similar patterns of CAZyme families but varied greatly in the number of genes within each category in the Carbohydrate-Active Enzymes database (CAZy), suggesting some level of functional redundancy. These results suggest that rumen Butyrivibrio species occupy similar niches but apply different degradation strategies to be able to coexist in the rumen.IMPORTANCE Feeding a global population of 8 billion people and climate change are the primary challenges facing agriculture today. Ruminant livestock are important food-producing animals, and maximizing their productivity requires an understanding of their digestive systems and the roles played by rumen microbes in plant polysaccharide degradation. Members of the genera Butyrivibrio and Pseudobutyrivibrio are a phylogenetically diverse group of bacteria and are commonly found in the rumen, where they are a substantial source of polysaccharide-degrading enzymes for the depolymerization of lignocellulosic material. Our findings have highlighted the immense enzymatic machinery of Butyrivibrio and Pseudobutyrivibrio species for the degradation of plant fiber, suggesting that these bacteria occupy similar niches but apply different degradation strategies in order to coexist in the competitive rumen environment.KEYWORDS: rumen, bacteria, polysaccharide, Butyrivibrio, Pseudobutyrivibrio, genome, CAZy, enolaseINTRODUCTIONThe need to feed a growing global population (1) is driving renewed interest in understanding the role of the rumen microbiota in the degradation and conversion of plant polysaccharides into high-value animal products (2). The rumen is one of the most efficient plant polysaccharide depolymerization and utilization systems known, and its microbes are promising sources of fibrolytic enzymes for application in the production of biofuels from lignocellulosic material (3). Rumen bacteria are responsible for most of the breakdown of plant fiber via close interactions among phylogenetically different, but physiologically complementary, bacterial species (4, 5). Species belonging to the genera Butyrivibrio and Pseudobutyrivibrio form a significant group of rumen bacteria (6, 7) and are among a small number of rumen microbes capable of utilizing xylans and pectins (8,–13). Butyrivibrio species contribute to fiber digestion in both animals (14,–17) and humans (18) due to their ability to degrade hemicelluloses (19,–22) and are also involved in protein breakdown (23) and the biohydrogenation of fatty acids (24, 25). At present, the genus Butyrivibrio includes the rumen species Butyrivibrio fibrisolvens, B. hungatei, and B. proteoclasticus and the human species B. crossotus (26,–30), while the genus Pseudobutyrivibrio has two species, Pseudobutyrivibrio xylanivorans and P. ruminis. Due to the substantial morphological (31), metabolic (32,–34), and serological (35, 36) differences, it is likely that more distinct species groups of Butyrivibrio and Pseudobutyrivibrio exist in the rumen.Butyrivibrio and Pseudobutyrivibrio strains encode a more impressive repertoire of carbohydrate-active enzymes (CAZymes) than most Firmicutes (7), including those involved in the degradation of pectin (glycoside hydrolase 28 [GH28], polysaccharide lyase 1 [PL1], PL9, PL10, PL11, carbohydrate esterase 8 [CE8], CE12) and xylan (GH8, GH10, GH11

机译：在瘤胃中的微生物植物植物多糖细分是在反刍动物牲畜中消化的基础。属于Rumen Genta Butyriiro和PseudobutyRivibrio的细菌物种是木质纤维素植物材料的重要降解剂和用具。这些细菌降解多糖和发酵释放的单糖，得到由反刍动物使用的短链脂肪酸，用于生长和生产肉类，牛奶和纤维产品。虽然瘤胃抑制和伪变质物种被认为是常见的瘤胃居民，但它们的多糖降解和碳水化合物利用酶尚不清楚。在这项研究中，我们分析了40个抑虫剂和6个伪曲叶菌菌株的基因组，以及从新西兰奶牛的植物粘附部分中分离的植物粘附部分，以探讨这些重要瘤胃细菌的多糖降解潜力。对比基因组分析与其16S rRNA基因的系统发育分析和短链脂肪酸生产模式提供了对这些细菌的基因组多样性和生理学的洞察，并将抑制剂分为3种簇。发现瘤胃抑制细菌是编码大型和多样化的降解碳水化合物 - 活性酶（巨曲型）和结合蛋白。总共4,421个糖苷水解酶（GHS），1,283个碳水化合物酯酶（CES），110个多糖裂解酶（PLS），3,605糖基三酶（GTS）和1,706个碳水化合物结合蛋白质模块（CBM），具有预测的涉及分解和运输的预测活动鉴定了不溶性植物多糖。抑虫基因组在碳水化合物 - 活性酶数据库（Cazy）中的每个类别中的基因数量中具有相似的巨大巨大系列，且暗示了一些功能冗余。这些结果表明，瘤胃抑制物种占据了类似的利基，但适用不同的降级策略，以便能够在瘤胃中共存。喂养全球人口80亿人口和气候变化是今天农业面临的主要挑战。反刍动物牲畜是重要的食品生产动物，并最大限度地提高其生产力需要了解他们的消化系统和瘤胃微生物在植物多糖降解中发挥的作用。 Genera Butyriiro和PseudobutyRivibrio的成员是一种系统源性多样的细菌，通常在瘤胃中发现，其中它们是用于木质纤维素材料的解聚的多糖降解酶的实质性来源。我们的研究结果强调了抑制抑制抑制纤维素和伪变大纤维物种的植物纤维的巨大酶机，这表明这些细菌占据了类似的利基，而是应用不同的降级策略，以便在竞争激烈的瘤胃环境中共存。：瘤词：瘤胃，细菌，多糖， ButyRivirio，Pseudobutirivirio，Genome，Cazy，EnolaseIntroduction喂养不断增长的全球人口（1）正在推动更新的兴趣了解瘤胃微生物的作用，在植物多糖降解和转化为高价值动物产品中（2）。瘤胃是已知最有效的植物多糖解聚和利用系统之一，其微生物是纤维溶解酶的有希望的纤维解酶来源，用于从木质纤维素材料（3）的生物燃料的生产中。瘤胃细菌对植物纤维的大部分崩溃负责，通过系统源性不同但生理互补，细菌物种（4,5）密切相互作用。属于Genta Butyriiro和PseudobutyRivib的物种形成了一组显着的瘤胃细菌（6,7），并且是能够利用Xylans和果胶（8，-13）的少量瘤胃微生物。抑制物种由于它们降解半纤维素（19，-22）并且还参与蛋白质分解（23）和脂肪酸的生物中水（脂肪酸的生物中）而导致纤维消化（18）的纤维消化有助于24,25）。目前，抑制属抑菌包括糊状物种纤维糊糊子纤维素，B. Hungatei和B. proteoclasticus和人类物种B.Crossotus（26,30），而Pseudobutirivirio Genus具有两个物种，伪失明的木聚糖血糖体和P.Ruminis。由于实质性（31），代谢（32，-34）和血清学（35,36）差异，可能在瘤胃中存在更明显的物种抑菌和伪变质纤维的抑菌和伪血管诱导菌株编码更多令人印象深刻的碳水化合物 - 活性酶（婴儿潮）比大多数常压（7），包括参与果胶降解的那些（糖苷水解酶28 [GH28]，多糖裂解酶1 [PL1]，PL9，PL10，PL11，碳水化合物酯酶8 [ CE8]，CE12）和XYLAN（GH8，GH10，GH11

Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities

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