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Promiscuous Enzymes Cause Biosynthesis of Diverse Siderophores in Shewanella oneidensis
Applied and Environmental Microbiology ( IF 3.9 ) Pub Date : 2020-03-18
Wang, S., Liang, H., Liu, L., Jiang, X., Wu, S., Gao, H.

The siderophore synthetic system in Shewanella species is able to synthesize dozens of macrocyclic siderophores in vitro with synthetic precursors. In vivo, however, although three siderophores are produced naturally in Shewanella algae B516, which carries a lysine decarboxylase (AvbA) specific for siderophore synthesis, only one siderophore can be detected from many other Shewanella species. In this study, we examined a siderophore-overproducing mutant of Shewanella oneidensis which lacks an AvbA counterpart, and we found that it can also produce these three siderophores. We identified both SpeC and SpeF as promiscuous decarboxylases for both lysine and ornithine to synthesize the siderophore precursors cadaverine and putrescine, respectively. Intriguingly, putrescine is mainly synthesized from arginine through an arginine decarboxylation pathway in a constitutive manner, not liable to the concentrations of iron and siderophores. Our results provide further evidence that the substrate availability plays a determining role in siderophore production. Furthermore, we provide evidence to suggest that under iron starvation conditions, cells allocate more putrescine for siderophore biosynthesis by downregulating the expression of the enzyme that transforms putrescine into spermidine. Overall, this study provides another example of the great flexibility of bacterial metabolism that is honed by evolution to better fit living environments of these bacteria.

IMPORTANCE The simultaneous production of multiple siderophores is considered a general strategy for microorganisms to rapidly adapt to their ever-changing environments. In this study, we show that some Shewanella spp. may downscale their capability for siderophore synthesis to facilitate adaptation. Although S. oneidensis lacks an enzyme specifically synthesizing cadaverine, it can produce it by using promiscuous ornithine decarboxylases. Despite this ability, this bacterium predominately produces the primary siderophore while restraining the production of secondary siderophores by regulating substrate availability. In addition to using the arginine decarboxylase (ADC) pathway for putrescine synthesis, cells optimize the putrescine pool for siderophore production. Our work provides an insight into the coordinated synthesis of multiple siderophores by harnessing promiscuous enzymes in bacteria and underscores the importance of substrate pools for the biosynthesis of natural products.



中文翻译:

混杂酶引起沙瓦氏假单胞菌不同铁载体的生物合成

希瓦氏菌属中的铁载体合成系统能够在体外与合成前体合成数十个大环铁载体。然而,在体内,尽管在希瓦氏菌藻类B516中天然产生了三个铁载体,它们携带着对铁氧体合成具有特异性的赖氨酸脱羧酶(AvbA),但是从许多其他希瓦氏菌种中只能检测到一个铁载体。在这项研究中,我们检查了Shewanella oneidensis的铁载体过量生产突变体。缺少AvbA对应物,我们发现它也可以产生这三种铁载体。我们确定SpeC和SpeF都是赖氨酸和鸟氨酸的混杂脱羧酶,分别合成铁载体前体尸胺和腐胺。有趣的是,腐胺主要由精氨酸通过精氨酸脱羧途径以本构方式从精氨酸合成,而不依赖于铁和铁载体的浓度。我们的结果提供了进一步的证据,证明底物的可用性在铁载体生产中起决定性作用。此外,我们提供的证据表明,在铁饥饿的条件下,细胞通过下调将腐胺转化为亚精胺的酶的表达来分配更多的腐胺用于铁载体的生物合成。总体,

重要信息多个铁载体的同时生产被认为是微生物快速适应其不断变化的环境的一般策略。在这项研究中,我们显示了一些希瓦氏菌属。可能降低其铁载体合成的能力以促进适应。虽然沙门氏菌缺乏专门合成尸胺的酶,它可以通过使用鸟氨酸脱羧酶来生产。尽管具有这种能力,但是该细菌主要产生初级铁载体,同时通过调节底物的可用性来抑制次级铁载体的产生。除了使用精氨酸脱羧酶(ADC)途径合成腐胺之外,细胞还优化了腐胺池以生产铁载体。我们的工作通过利用细菌中的混杂酶为多种铁载体的协调合成提供了见识,并强调了底物库对于天然产物生物合成的重要性。

更新日期:2020-03-19
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