Adaptive Remodeling of the Bacterial Proteome by Specific Ribosomal Modification Regulates Pseudomonas Infection and Niche Colonisation.
Adaptive Remodeling of the Bacterial Proteome by Specific Ribosomal Modification Regulates Pseudomonas Infection and Niche Colonisation.
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DOI：
10.1371/journal.pgen.1005837
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发表时间：
2016-02
期刊：
影响因子：
4.5
通讯作者：
Malone JG
中科院分区：
文献类型：
--
作者：
Little RH;Grenga L;Saalbach G;Howat AM;Pfeilmeier S;Trampari E;Malone JG
蛋白质丰度的转录后调控是一个非常重要的，但尚未充分研究的调控过程，生物体通过该过程对其环境作出反应。在这里，我们描述了一个重要的和以前未确定的监管途径，涉及核糖体修饰蛋白RimK，其调节蛋白RimA和RimB，和广泛的细菌第二信使环二GMP（cdG）。rimK的破坏影响致病性假单胞菌和铜绿假单胞菌物种的运动性和表面附着，其中rimK缺失显著地损害了根际土壤细菌荧光假单胞菌的定殖，以及病原体铜绿假单胞菌和铜绿假单胞菌的植物感染。RimK作为ATP依赖性谷氨酰连接酶发挥作用，将谷氨酸残基添加到核糖体蛋白RpsF的C末端，并诱导对核糖体蛋白补体和功能的特异性作用。荧光假单胞菌中rimK的缺失导致多种核糖体蛋白的水平显著降低，并且还导致关键翻译调节因子Hfq的水平显著降低。反过来，降低的Hfq水平诱导特异性下游蛋白质组学变化，在ΔrimK和Δhfq突变体中观察到多种ABC转运蛋白、应激反应蛋白和非核糖体肽合成酶的显著增加。RimK的活性本身由与RimA、RimB和cdG的相互作用控制。我们提出，RimK活性的控制代表了一种新的调控机制，动态影响细菌和它们的宿主之间的相互作用，翻译环境压力到动态的核糖体变化，从而适应性重塑细菌蛋白质组。蛋白质丰度的转录后调控是生物体响应环境变化的一个重要而又未充分研究的调控过程。我们已经发现了一个重要的新机制，这种控制在细菌中，基于共价修饰的小核糖体蛋白的广泛酶RimK。在这里，我们表明RimK的活性对细胞中核糖体蛋白的水平具有特定的影响，这反过来又影响重要的翻译调节因子Hfq的丰度。RimK本身通过与小调节蛋白RimA和RimB以及广泛分布的信号分子cyclic-di-GMP结合来控制。rimK的缺失损害了几种不同假单胞菌属物种的运动性、毒力和植物定殖/感染。我们建议，细胞内RimK活性的变化，使假单胞菌响应环境压力，通过改变其核糖体的性质，从而导致适应性表型响应其周围环境。这在植物接触的初始阶段促进运动性和毒性，并且在长期环境适应期间促进表型，包括附着、代谢物运输和胁迫控制。
Post-transcriptional control of protein abundance is a highly important, underexplored regulatory process by which organisms respond to their environments. Here we describe an important and previously unidentified regulatory pathway involving the ribosomal modification protein RimK, its regulator proteins RimA and RimB, and the widespread bacterial second messenger cyclic-di-GMP (cdG). Disruption of rimK affects motility and surface attachment in pathogenic and commensal Pseudomonas species, with rimK deletion significantly compromising rhizosphere colonisation by the commensal soil bacterium P. fluorescens, and plant infection by the pathogens P. syringae and P. aeruginosa. RimK functions as an ATP-dependent glutamyl ligase, adding glutamate residues to the C-terminus of ribosomal protein RpsF and inducing specific effects on both ribosome protein complement and function. Deletion of rimK in P. fluorescens leads to markedly reduced levels of multiple ribosomal proteins, and also of the key translational regulator Hfq. In turn, reduced Hfq levels induce specific downstream proteomic changes, with significant increases in multiple ABC transporters, stress response proteins and non-ribosomal peptide synthetases seen for both ΔrimK and Δhfq mutants. The activity of RimK is itself controlled by interactions with RimA, RimB and cdG. We propose that control of RimK activity represents a novel regulatory mechanism that dynamically influences interactions between bacteria and their hosts; translating environmental pressures into dynamic ribosomal changes, and consequently to an adaptive remodeling of the bacterial proteome. Post-transcriptional control of protein abundance is a significant and underexplored regulatory process by which organisms respond to environmental change. We have discovered an important new mechanism for this control in bacteria, based on the covalent modification of a small ribosomal protein by the widespread enzyme RimK. Here we show that the activity of RimK has specific effects on the levels of ribosomal proteins in the cell, which in turn affects the abundance of the important translational regulator Hfq. RimK is itself controlled by binding to the small regulatory proteins RimA and RimB and the widespread signalling molecule cyclic-di-GMP. Deletion of rimK compromises motility, virulence and plant colonisation/infection in several different Pseudomonas species. We propose that changes in intracellular RimK activity enable Pseudomonas to respond to environmental pressures by changing the nature of their ribosomes, leading in turn to an adaptive phenotypic response to their surroundings. This promotes motility and virulence during the initial stages of plant contact, and phenotypes including attachment, metabolite transport and stress control during long-term environmental adaptation.