Ecological Importance of Cross-Feeding of the Intermediate Metabolite 1,2-Propanediol between Bacterial Gut Symbionts

Ecological Importance of Cross-Feeding of the Intermediate Metabolite 1,2-Propanediol between Bacterial Gut Symbionts
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DOI:
10.1128/aem.00190-20
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发表时间:
2020-06-01
影响因子:
4.4
通讯作者:
Walter, Jens
Walter, Jens
中科院分区:
生物学2区
文献类型:
--
作者:
Cheng, Christopher C.;Duar, Rebbeca;Walter, Jens

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基于代谢产物1,2-丙二醇的交叉摄食已被提出在建立肠道共生体之间的营养相互作用中具有重要作用,但其生态学重要性尚未被经验性地确立。在这里,我们表明,在体外生长的罗伊氏乳杆菌(syn。通过短双歧杆菌UCC 2003和大肠杆菌MG 1655分别从岩藻糖和鼠李糖的代谢产生1,2-丙二醇来增强罗伊氏乳杆菌ATCC PTA 6475。对同基因突变体的研究表明,营养相互作用依赖于L. reuteri,其编码使用1,2-丙二醇的能力,以及B中的L-岩藻糖通透酶(fucP)基因。短,其是从岩藻糖形成1,2-丙二醇所需的。在gnotobiotic小鼠中的实验表明,尽管pduCDE操纵子赋予L. reuteri ATCC PTA 6475在小鼠消化道中,菌株的生态性能在B存在下增强。breve UCC 2003和粘液降解种两歧双歧杆菌。使用L. reuteri和B.在小鼠实验中的Breve表明,营养相互作用特别基于1,2-丙二醇。总之,我们的工作建立了基于1,2-丙二醇的交叉喂养关系对于脊椎动物肠道中细菌共生体的适应性的生态重要性。(短双歧杆菌)和利用(罗伊氏乳杆菌)1,2-丙二醇,这项研究提供了机制洞察肠道共生体之间的营养相互作用的生态后果。这一发现加深了我们对交叉喂养如何影响L. reuteri在脊椎动物的肠道,并揭示了一个假定的选择力,塑造了物种的进化。这些发现是相关的,因为它们为设计合理的基于微生物的策略以调节肠道生态系统提供了基础,这些策略可以采用建立营养相互作用的细菌菌株混合物,或者基于常驻微生物群为传入微生物提供资源的能力的个性化方法。
Cross-feeding based on the metabolite 1,2-propanediol has been proposed to have an important role in the establishment of trophic interactions among gut symbionts, but its ecological importance has not been empirically established. Here, we show that in vitro growth of Lactobacillus reuteri (syn. Limosilactobacillus reuteri) ATCC PTA 6475 is enhanced through 1,2-propanediol produced by Bifidobacterium breve UCC2003 and Escherichia coli MG1655 from the metabolization of fucose and rhamnose, respectively. Work with isogenic mutants showed that the trophic interaction is dependent on the pduCDE operon in L. reuteri, which encodes the ability to use 1,2-propanediol, and the L-fucose permease (fucP) gene in B. breve, which is required for 1,2-propanediol formation from fucose. Experiments in gnotobiotic mice revealed that, although the pduCDE operon bestows a fitness burden on L. reuteri ATCC PTA 6475 in the mouse digestive tract, the ecological performance of the strain was enhanced in the presence of B. breve UCC2003 and the mucus-degrading species Bifidobacterium bifidum. The use of the respective pduCDE and fucP mutants of L. reuteri and B. breve in the mouse experiments indicated that the trophic interaction was specifically based on 1,2-propanediol. Overall, our work established the ecological importance of cross-feeding relationships based on 1,2-propanediol for the fitness of a bacterial symbiont in the vertebrate gut.IMPORTANCE Through experiments in gnotobiotic mice that employed isogenic mutants of bacterial strains that produce (Bifidobacterium breve) and utilize (Lactobacillus reuteri) 1,2-propanediol, this study provides mechanistic insight into the ecological ramifications of a trophic interaction between gut symbionts. The findings improve our understanding on how cross-feeding influences the competitive fitness of L. reuteri in the vertebrate gut and revealed a putative selective force that shaped the evolution of the species. The findings are relevant since they provide a basis to design rational microbial-based strategies to modulate gut ecosystems, which could employ mixtures of bacterial strains that establish trophic interactions or a personalized approach based on the ability of a resident microbiota to provide resources for the incoming microbe.