Syntrophic splitting of central carbon metabolism in host cells bearing functionally different symbiotic bacteria
Syntrophic splitting of central carbon metabolism in host cells bearing functionally different symbiotic bacteria
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DOI：
10.1038/s41396-020-0661-z
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发表时间：
2020-04-29
期刊：
影响因子：
11
通讯作者：
Douglas, Angela E.
中科院分区：
文献类型：
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作者：
Ankrah, Nana Y. D.;Wilkes, Rebecca A.;Douglas, Angela E.
以木质部植物汁液营养贫乏的饮食为食的昆虫通常携带两种微生物共生体，它们定位于不同的器官（细菌组）并提供互补的必需氨基酸（EAA）。在这里，我们调查的代谢基础明显的悖论，木质部喂养的昆虫是在激烈的选择代谢效率，但产生的成本维持两个共生体的功能介导的一个共生体在其他协会。使用稳定同位素分析的中心碳代谢和代谢建模，我们提供的证据表明，细菌的spittlebug的变形杆菌显示高速率的有氧糖酵解，与葡萄糖氧化的互养分裂。具体来说，我们的数据表明，一个细菌组（含有细菌Sulcia，它合成七个EAA）主要处理葡萄糖酵解，产生丙酮酸和乳酸，和出口的丙酮酸和乳酸被第二个细菌组（含有细菌Zinderia，它合成三个能量昂贵的EAA）同化，并通过TCA循环通过氧化磷酸化产生能量。此外，我们计算，这种代谢安排支持高ATP的需求，在Zinderia菌群Zinderia介导的合成能量密集型EAA。我们预测，宿主细胞之间的代谢物交叉喂养可能广泛存在于利用低营养饮食的动物-微生物共生体中。
Insects feeding on the nutrient-poor diet of xylem plant sap generally bear two microbial symbionts that are localized to different organs (bacteriomes) and provide complementary sets of essential amino acids (EAAs). Here, we investigate the metabolic basis for the apparent paradox that xylem-feeding insects are under intense selection for metabolic efficiency but incur the cost of maintaining two symbionts for functions mediated by one symbiont in other associations. Using stable isotope analysis of central carbon metabolism and metabolic modeling, we provide evidence that the bacteriomes of the spittlebug Clastoptera proteus display high rates of aerobic glycolysis, with syntrophic splitting of glucose oxidation. Specifically, our data suggest that one bacteriome (containing the bacterium Sulcia, which synthesizes seven EAAs) predominantly processes glucose glycolytically, producing pyruvate and lactate, and the exported pyruvate and lactate is assimilated by the second bacteriome (containing the bacterium Zinderia, which synthesizes three energetically costly EAAs) and channeled through the TCA cycle for energy generation by oxidative phosphorylation. We, furthermore, calculate that this metabolic arrangement supports the high ATP demand in Zinderia bacteriomes for Zinderia-mediated synthesis of energy-intensive EAAs. We predict that metabolite cross-feeding among host cells may be widespread in animal-microbe symbioses utilizing low-nutrient diets.