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Microbial Succession of Anaerobic Chitin Degradation in Freshwater Sediments

机译:淡水沉积物中厌氧甲壳质降解的微生物演替

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Chitin is massively produced by freshwater plankton species as a structural element of their exoskeleton or cell wall. At the same time, chitin does not accumulate in the predominantly anoxic sediments, underlining its importance as carbon and nitrogen sources for sedimentary microorganisms. We studied chitin degradation in littoral sediment of Lake Constance, Central Europe’s third largest lake. Turnover of the chitin analog methyl-umbelliferyl-N,N-diacetylchitobioside (MUF-DC) was highest in the upper oxic sediment layer, with 5.4?nmol MUF-DC h?1 (g sediment [dry weight])?1. In the underlying anoxic sediment layers, chitin hydrolysis decreased with depth from 1.1 to 0.08?nmol MUF-DC h?1 (g sediment [dry weight])?1. Bacteria involved in chitin degradation were identified by 16S rRNA (gene) amplicon sequencing of anoxic microcosms incubated in the presence of chitin compared to microcosms amended either with N-acetylglucosamine as the monomer of chitin or no substrate. Chitin degradation was driven by a succession of bacteria responding specifically to chitin only. The early phase (0 to 9?days) was dominated by Chitinivibrio spp. (Fibrobacteres). The intermediate phase (9 to 21?days) was characterized by a higher diversity of chitin responders, including, besides Chitinivibrio spp., also members of the phyla Bacteroidetes, Proteobacteria, Spirochaetes, and Chloroflexi. In the late phase (21 to 43?days), the Chitinivibrio populations broke down with a parallel strong increase of Ruminiclostridium spp. (formerly Clostridium cluster III, Firmicutes), which became the dominating chitin responders. Our study provides quantitative insights into anaerobic chitin degradation in lake sediments and linked this to a model of microbial succession associated with this activity.IMPORTANCE Chitin is the most abundant biopolymer in aquatic environments, with a direct impact on the carbon and nitrogen cycles. Despite its massive production as a structural element of crustaceans, insects, or algae, it does not accumulate in sediments. Little is known about its turnover in predominantly anoxic freshwater sediments and the responsible microorganisms. We proved that chitin is readily degraded under anoxic conditions and linked this to a succession of the members of the responsible microbial community over a 43-day period. While Fibrobacteres and Firmicutes members were driving the early and late phases of chitin degradation, respectively, a more diverse community was involved in chitin degradation in the intermediate phase. Entirely different microorganisms responded toward the chitin monomer N-acetylglucosamine, which underscores that soluble monomers are poor and misleading substrates to study polymer-utilizing microorganisms. Our study provides quantitative insights into the microbial ecology driving anaerobic chitin degradation in freshwater sediments.
机译:几丁质由淡水浮游生物物种大量生产,作为其外骨骼或细胞壁的结构元素。同时,几丁质不会在主要缺氧的沉积物中聚集,从而强调了其作为沉积微生物的碳源和氮源的重要性。我们研究了中欧第三大湖泊康斯坦茨湖沿岸沉积物中的几丁质降解。甲壳素类似物甲基伞形基-N,N-二乙酰基壳聚糖的苷(MUF-DC)在上层含氧沉积层中的周转量最高,为5.4?nmol MUF-DC h?1(克沉积物[干重])?1。在下面的缺氧沉积物层中,几丁质水解深度从1.1降至0.08nmol MUF-DC h-1(克沉积物[干重])-1。通过在壳多糖存在下孵育的缺氧微观世界的16S rRNA(基因)扩增子测序,与用N-乙酰氨基葡糖作为几丁质单体修饰的微观世界相比,鉴定了参与几丁质降解的细菌。几丁质降解是由一系列仅对几丁质特异反应的细菌驱动的。早期阶段(0到9天)主要是Chitinivibrio spp。 (纤维杆菌)。中间阶段(9至21天)的特点是几丁质反应者的多样性更高,除Chitinivibrio spp。外,还包括拟杆菌属,变形杆菌,螺旋体和绿叶弯曲菌的成员。在后期(21至43天),Chitinivibrio种群破裂,而Ruminiclostridium spp则同时强劲增长。 (以前称为梭菌群III,Firmicutes),它成为主要的几丁质响应者。我们的研究提供了关于湖泊沉积物中厌氧甲壳质降解的定量见解,并将其与与此活动相关的微生物演替模型联系起来。重要信息甲壳质是水生环境中最丰富的生物聚合物,直接影响碳和氮的循环。尽管其大量生产为甲壳类,昆虫或藻类的结构元素,但它并未积聚在沉积物中。关于其在主要为缺氧的淡水沉积物和负责任微生物中的周转率知之甚少。我们证明了甲壳素在缺氧条件下很容易降解,并将其与负责的微生物群落成员在43天的时间内相联系。当纤维杆菌和Firmicutes成员分别驱动甲壳质降解的早期和晚期阶段时,中间阶段的甲壳质降解涉及更多​​样化的社区。完全不同的微生物对几丁质单体N-乙酰氨基葡萄糖有反应,这说明可溶性单体很差,并且在研究利用聚合物的微生物时会误导底物。我们的研究为微生物生态学驱动淡水沉积物中厌氧甲壳质降解提供了定量的见解。

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