Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP

Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP
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DOI:
10.1128/jb.188.7.2681-2691.2006
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发表时间:
2006-04-01
影响因子:
3.2
通讯作者:
Spormann, AM
Spormann, AM
中科院分区:
生物学3区
文献类型:
--
作者:
Thormann, KM;Duttler, S;Spormann, AM

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对环境扰动的稳定性和恢复力是医疗和环境生物膜的关键特性,并为它们的控制提出了重要目标。生物膜的稳定性由两个相互排斥的过程决定:细胞附着于生物膜基质和从生物膜基质脱离。使用希瓦氏菌(Shewanella oneidensis)MR-1(一种环境通用的Fe(III)和Mn(IV)矿物质还原微生物),我们将mxdABCD鉴定为形成三维生物膜所必需的一组新基因。分子分析显示,mxdA编码具有不寻常的GGDEF基序的环状双(3 ',5')鸟苷酸(环状二-GMP)形成酶,即,NVDEF,这对其功能至关重要。mxdB编码推定的膜相关糖基转移酶。这两种基因都是基质附着所必需的。Δ mxdA突变体的附着缺陷表型通过VCA 0956的异位表达而被拯救,VCA 0956编码另一种二鸟苷酸环化酶。有趣的是,在诱导yhjH(一种编码已显示具有磷酸二酯酶活性的酶的基因)后,发生了从生物膜的快速细胞脱离。以这种方式,有可能绕过先前确定的分子氧突然耗尽作为诱导生物膜溶解的环境触发因素。我们提出了c-di-GMP作为关键细胞内调节剂的模型,用于通过以浓度依赖性方式在附着和脱离之间转移生物膜细胞的状态来控制生物膜稳定性。
Stability and resilience against environmental perturbations are critical properties of medical and environmental biofilms and pose important targets for their control. Biofilm stability is determined by two mutually exclusive processes: attachment of cells to and detachment from the biofilm matrix. Using Shewanella oneidensis MR-1, an environmentally versatile, Fe(III) and Mn(IV)) mineral -reducing microorganism, we identified mxdABCD as a new set of genes essential for formation of a three-dimensional biofilm. Molecular analysis revealed that mxdA encodes a cyclic bis(3',5')guanylic acid (cyclic di-GMP)-forming enzyme with an unusual GGDEF motif, i.e., NVDEF, which is essential for its function. mxdB encodes a putative membrane-associated glycosyl transferase. Both genes are essential for matrix attachment. The attachment- deficient phenotype of a Delta mxdA mutant was rescued by ectopic expression of VCA0956, encoding another diguanylate cyclase. Interestingly, a rapid cellular detachment from the biofilm occurred upon induction of yhjH, a gene encoding an enzyme that has been shown to have phosphodiesterase activity. In this way, it was possible to bypass the previously identified sudden depletion of molecular oxygen as an environmental trigger to induce biofilm dissolution. We propose a model for c-di-GMP as a key intracellular regulator for controlling biofilm stability by shifting the state of a biofilm cell between attachment and detachment in a concentration -dependent manner.