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Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr(VI) immobilization.

ABSTRACT: Although biofilm-based bioprocesses have been increasingly used in various applications, the long-term robust and efficient biofilm performance remains one of the main bottlenecks. In this study, we demonstrated that biofilm cohesiveness and performance of Shewanella oneidensis can be enhanced through disrupting putrescine biosynthesis. Through random transposon mutagenesis library screening, one hyperadherent mutant strain, CP2-1-S1, exhibiting an enhanced capability in biofilm formation, was obtained. Comparative analysis of the performance of biofilms formed by S. oneidensis MR-1 wild type (WT) and CP2-1-S1 in removing dichromate (Cr2O7(2-)), i.e., Cr(VI), from the aqueous phase showed that, compared with the WT biofilms, CP2-1-S1 biofilms displayed a substantially lower rate of cell detachment upon exposure to Cr(VI), suggesting a higher cohesiveness of the mutant biofilms. In addition, the amount of Cr(III) immobilized by CP2-1-S1 biofilms was much larger, indicating an enhanced performance in Cr(VI) bioremediation. We further showed that speF, a putrescine biosynthesis gene, was disrupted in CP2-1-S1 and that the biofilm phenotypes could be restored by both genetic and chemical complementations. Our results also demonstrated an important role of putrescine in mediating matrix disassembly in S. oneidensis biofilms.

SUBMITTER: Ding Y

PROVIDER: S-EPMC3911039 | biostudies-literature | 2014 Feb

REPOSITORIES: biostudies-literature

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Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr(VI) immobilization.

Ding Yuanzhao Y Peng Ni N Du Yonghua Y Ji Lianghui L Cao Bin B

Applied and environmental microbiology 20131220 4

Although biofilm-based bioprocesses have been increasingly used in various applications, the long-term robust and efficient biofilm performance remains one of the main bottlenecks. In this study, we demonstrated that biofilm cohesiveness and performance of Shewanella oneidensis can be enhanced through disrupting putrescine biosynthesis. Through random transposon mutagenesis library screening, one hyperadherent mutant strain, CP2-1-S1, exhibiting an enhanced capability in biofilm formation, was o ...[more]

PMID: 24362428

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Project description: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.

Dataset Information

Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr(VI) immobilization.

Publications

Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr(VI) immobilization.

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