Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts.

Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts.
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DOI:
10.1371/journal.pbio.1001221
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发表时间:
2011-12
期刊:
影响因子:
9.8
通讯作者:
Gordon JI
Gordon JI
中科院分区:
生物学1区
文献类型:
--
作者:
Martens EC;Lowe EC;Chiang H;Pudlo NA;Wu M;McNulty NP;Abbott DW;Henrissat B;Gilbert HJ;Bolam DN;Gordon JI

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对不同类型的植物细胞壁相关多糖中所含营养物质的竞争可以解释人类肠道微生物群中常见细菌成员中底物特异性分解代谢基因模块的进化。栖息在人类肠道中的共生细菌在巨大的压力下进化,以利用复杂的碳水化合物,主要是我们饮食中的植物细胞壁聚糖。这些多糖不被人体酶消化,但被肠道细菌加工成可吸收的短链脂肪酸。拟杆菌门是成年人肠道中两个主要的细菌门之一,具有广泛的聚糖降解能力。这些物种使用一系列膜蛋白复合物,称为Sus-like系统,用于催化许多复杂的碳水化合物。然而,这些系统在降解植物细胞壁聚糖的化学多样性库中的作用仍然未知。在这里,我们表明,两个密切相关的人类肠道拟杆菌,B。多形核和B。卵形酵母能够利用几乎所有的主要植物和宿主聚糖,包括鼠李糖半乳糖醛酸聚糖II,一种被认为对微生物降解具有抑制作用的高度复杂的聚合物。转录谱分析和基因失活实验揭示了多糖利用位点(普尔斯)的身份和特异性,编码个人的Sus-like系统,针对各种植物多糖。比较基因组分析表明,B. ovatus具有几种独特的普尔斯,其能够降解半纤维素多糖,这是B中不存在的表型。太多了。相反,B.多形核基因组已经通过参与宿主粘蛋白O-聚糖代谢的普尔斯数量增加而成形,所述表型在B中不可检测。卵形的PUL相关的混合双组分系统的纯化传感器结构域结合转录分析的研究表明,复杂的寡糖提供的监管线索,诱导PUL激活,每个PUL是高度特定的细胞壁聚合物。这些结果提供了这些物种如何通过进化针对独特的可用多糖的基因而分化成不同的碳水化合物生态位的观点,这一主题可能适用于来自肠道和其他栖息地的不同细菌。栖息在人类肠道中的细菌对于消化构成膳食纤维的植物源聚糖至关重要。人体产生的酶不能降解这些丰富的膳食成分,如果没有细菌的帮助,它们就会被闲置。我们研究了两个物种所采用的分子策略,这两个物种属于人类结肠中最丰富的细菌群之一(拟杆菌)。我们的研究结果表明,每个物种都进化到降解一个独特的聚糖子集;这种专业化反映在各自的基因组中,每个基因组都包含许多独立的基因簇,参与代谢植物纤维多糖或分泌粘液中的聚糖。每个聚糖特异性基因簇产生一系列相关的膜相关蛋白,这些蛋白一起用于结合和降解特定的聚糖。每个聚糖特异性基因簇的表达由环境传感器控制,该环境传感器响应于其靶向的底物中所含的独特分子特征的存在。这些结果提供了相关细菌物种如何通过进化感测和降解可用多糖的独特套件的基因而分化成不同的碳水化合物生态位的观点,这一过程可能适用于来自肠道和其他栖息地的不同细菌。
Competition for nutrients contained in diverse types of plant cell wall-associated polysaccharides may explain the evolution of substrate-specific catabolic gene modules in common bacterial members of the human gut microbiota. Symbiotic bacteria inhabiting the human gut have evolved under intense pressure to utilize complex carbohydrates, primarily plant cell wall glycans in our diets. These polysaccharides are not digested by human enzymes, but are processed to absorbable short chain fatty acids by gut bacteria. The Bacteroidetes, one of two dominant bacterial phyla in the adult gut, possess broad glycan-degrading abilities. These species use a series of membrane protein complexes, termed Sus-like systems, for catabolism of many complex carbohydrates. However, the role of these systems in degrading the chemically diverse repertoire of plant cell wall glycans remains unknown. Here we show that two closely related human gut Bacteroides, B. thetaiotaomicron and B. ovatus, are capable of utilizing nearly all of the major plant and host glycans, including rhamnogalacturonan II, a highly complex polymer thought to be recalcitrant to microbial degradation. Transcriptional profiling and gene inactivation experiments revealed the identity and specificity of the polysaccharide utilization loci (PULs) that encode individual Sus-like systems that target various plant polysaccharides. Comparative genomic analysis indicated that B. ovatus possesses several unique PULs that enable degradation of hemicellulosic polysaccharides, a phenotype absent from B. thetaiotaomicron. In contrast, the B. thetaiotaomicron genome has been shaped by increased numbers of PULs involved in metabolism of host mucin O-glycans, a phenotype that is undetectable in B. ovatus. Binding studies of the purified sensor domains of PUL-associated hybrid two-component systems in conjunction with transcriptional analyses demonstrate that complex oligosaccharides provide the regulatory cues that induce PUL activation and that each PUL is highly specific for a defined cell wall polymer. These results provide a view of how these species have diverged into different carbohydrate niches by evolving genes that target unique suites of available polysaccharides, a theme that likely applies to disparate bacteria from the gut and other habitats. Bacteria inhabiting the human gut are critical for digestion of the plant-derived glycans that compose dietary fiber. Enzymes produced by the human body cannot degrade these abundant dietary components, and without bacterial assistance they would go unused. We investigated the molecular strategies employed by two species belonging to one of the most abundant bacterial groups in the human colon (the Bacteroidetes). Our results show that each species has evolved to degrade a unique subset of glycans; this specialization is reflected in their respective genomes, each of which contains numerous separate gene clusters involved in metabolizing plant fiber polysaccharides or glycans present in secreted mucus. Each glycan-specific gene cluster produces a related series of membrane-associated proteins which together serve to bind and degrade a specific glycan. Expression of each glycan-specific gene cluster is controlled by an environmental sensor that responds to the presence of a unique molecular signature contained in the substrate that it targets. These results provide a view of how related bacterial species have diverged into different carbohydrate niches by evolving genes that sense and degrade unique suites of available polysaccharides, a process that likely applies to disparate bacteria from the gut and other habitats.
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发表时间: 2010-03-04
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影响因子: 64.8
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通讯作者: --
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