pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures.

pH-Mediated Microbial and Metabolic Interactions in Fecal Enrichment Cultures.
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DOI:
10.1128/msphere.00047-17
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发表时间:
2017-05
期刊:
影响因子:
4.8
通讯作者:
Krajmalnik-Brown R
Krajmalnik-Brown R
中科院分区:
生物学2区
文献类型:
--
作者:
Ilhan ZE;Marcus AK;Kang DW;Rittmann BE;Krajmalnik-Brown R

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人的肠道是一个动态的环境,微生物通过其代谢产物与宿主持续相互作用。一些最重要的微生物代谢产物是发酵产物,如短链脂肪酸。这些发酵产物的产生和发酵微生物区系的流行取决于pH、碱度和可利用的膳食糖,但关于它们的代谢相互作用的细节尚不清楚。在这里,我们表明,在体外条件下,pH是微生物群落结构和功能以及对pH敏感的发酵菌种之间的微生物和代谢相互作用的最强驱动因素。碳酸氢盐的碱度和发酵形成的脂肪酸之间的平衡决定了控制微生物群落结构的pH值。我们的结果强调了pH平衡对不同微生物生态系统(如人类肠道)中微生物功能的影响。PH和可发酵底物对肠道微生物群落及其代谢施加选择性压力。我们使用三种分批培养方法评估了pH、碱度和底物对微生物群落结构、新陈代谢和功能相互作用的相对贡献。这些分批培养从粪浆开始,初始pH分别为6.0、6.5或6.9,以葡萄糖、果糖或纤维二糖为碳底物。对16S rRNA基因序列和发酵产物进行了分析。微生物多样性受pH和底物类型的共同影响。由于碱度不足,pH从6.0降到~4.5时,pH 6.0的培养物聚集在一起,而远离pH 6.5和6.9的培养物,这两种培养物只经历了很小的pH下降。纤维二糖产生的酸性大于碱性,这是由于可发酵碳的数量,这使得纤维二糖pH 6.5培养物远离其他pH 6.5培养物。PH对微生物群落结构的影响主要体现在发酵代谢上。乳酸的积累发生在pH 6.0的培养中,而丙酸和醋酸盐的积累在pH 6.5和6.9的培养中观察到,并且与所提供的底物的类型无关。最后,pH对乳酸盐生产和消费群落之间的相互作用产生了影响。产乳酸链球菌以pH 6.0为主,产乙酸酯和丙酸的韦洛氏菌、类杆菌和埃希氏菌占主导地位,起始pH为6.5和6.9。对乳酸消耗物种的酸抑制导致乳酸积累。我们的结果提供了对发酵微生物区系中pH衍生的变化和人类肠道中的代谢的见解。重要性人体肠道是一个动态的环境,微生物通过其代谢产物与宿主持续相互作用。一些最重要的微生物代谢产物是发酵产物,如短链脂肪酸。这些发酵产物的产生和发酵微生物区系的流行取决于pH、碱度和可利用的膳食糖,但关于它们的代谢相互作用的细节尚不清楚。在这里,我们表明,在体外条件下,pH是微生物群落结构和功能以及对pH敏感的发酵菌种之间的微生物和代谢相互作用的最强驱动因素。碳酸氢盐的碱度和发酵形成的脂肪酸之间的平衡决定了控制微生物群落结构的pH值。我们的结果强调了pH平衡对不同微生物生态系统(如人类肠道)中微生物功能的影响。
The human gut is a dynamic environment in which microorganisms consistently interact with the host via their metabolic products. Some of the most important microbial metabolic products are fermentation products such as short-chain fatty acids. Production of these fermentation products and the prevalence of fermenting microbiota depend on pH, alkalinity, and available dietary sugars, but details about their metabolic interactions are unknown. Here, we show that, for in vitro conditions, pH was the strongest driver of microbial community structure and function and microbial and metabolic interactions among pH-sensitive fermentative species. The balance between bicarbonate alkalinity and formation of fatty acids by fermentation determined the pH, which controlled microbial community structure. Our results underscore the influence of pH balance on microbial function in diverse microbial ecosystems such as the human gut. pH and fermentable substrates impose selective pressures on gut microbial communities and their metabolisms. We evaluated the relative contributions of pH, alkalinity, and substrate on microbial community structure, metabolism, and functional interactions using triplicate batch cultures started from fecal slurry and incubated with an initial pH of 6.0, 6.5, or 6.9 and 10 mM glucose, fructose, or cellobiose as the carbon substrate. We analyzed 16S rRNA gene sequences and fermentation products. Microbial diversity was driven by both pH and substrate type. Due to insufficient alkalinity, a drop in pH from 6.0 to ~4.5 clustered pH 6.0 cultures together and distant from pH 6.5 and 6.9 cultures, which experienced only small pH drops. Cellobiose yielded more acidity than alkalinity due to the amount of fermentable carbon, which moved cellobiose pH 6.5 cultures away from other pH 6.5 cultures. The impact of pH on microbial community structure was reflected by fermentative metabolism. Lactate accumulation occurred in pH 6.0 cultures, whereas propionate and acetate accumulations were observed in pH 6.5 and 6.9 cultures and independently from the type of substrate provided. Finally, pH had an impact on the interactions between lactate-producing and -consuming communities. Lactate-producing Streptococcus dominated pH 6.0 cultures, and acetate- and propionate-producing Veillonella, Bacteroides, and Escherichia dominated the cultures started at pH 6.5 and 6.9. Acid inhibition on lactate-consuming species led to lactate accumulation. Our results provide insights into pH-derived changes in fermenting microbiota and metabolisms in the human gut. IMPORTANCE The human gut is a dynamic environment in which microorganisms consistently interact with the host via their metabolic products. Some of the most important microbial metabolic products are fermentation products such as short-chain fatty acids. Production of these fermentation products and the prevalence of fermenting microbiota depend on pH, alkalinity, and available dietary sugars, but details about their metabolic interactions are unknown. Here, we show that, for in vitro conditions, pH was the strongest driver of microbial community structure and function and microbial and metabolic interactions among pH-sensitive fermentative species. The balance between bicarbonate alkalinity and formation of fatty acids by fermentation determined the pH, which controlled microbial community structure. Our results underscore the influence of pH balance on microbial function in diverse microbial ecosystems such as the human gut.