Center for Systems Biology, Harvard University, 52 Oxford St, Cambridge, MA 02138, USA.
Mol Microbiol. 2011 Jan;79(1):166-79. doi: 10.1111/j.1365-2958.2010.07436.x. Epub 2010 Nov 2.
Bacterial populations frequently act as a collective by secreting a wide range of compounds necessary for cell-cell communication, host colonization and virulence. How such behaviours avoid exploitation by spontaneous 'cheater' mutants that use but do not contribute to secretions remains unclear. We investigate this question using Pseudomonas aeruginosa swarming, a collective surface motility requiring massive secretions of rhamnolipid biosurfactants. We first show that swarming is immune to the evolution of rhlA(-) 'cheaters'. We then demonstrate that P. aeruginosa resists cheating through metabolic prudence: wild-type cells secrete biosurfactants only when the cost of their production and impact on individual fitness is low, therefore preventing non-secreting strains from gaining an evolutionary advantage. Metabolic prudence works because the carbon-rich biosurfactants are only produced when growth is limited by another growth limiting nutrient, the nitrogen source. By genetically manipulating a strain to produce the biosurfactants constitutively we show that swarming becomes cheatable: a non-producing strain rapidly outcompetes and replaces this obligate cooperator. We argue that metabolic prudence, which may first evolve as a direct response to cheating or simply to optimize growth, can explain the maintenance of massive secretions in many bacteria. More generally, prudent regulation is a mechanism to stabilize cooperation.
细菌群体经常通过分泌广泛的化合物来进行集体行动，这些化合物对于细胞间通讯、宿主定殖和毒力至关重要。然而，这些行为如何避免被自发的“骗子”突变体利用，这些突变体只利用但不贡献分泌物，目前仍不清楚。我们使用铜绿假单胞菌的群集运动来研究这个问题，这是一种需要大量分泌鼠李糖脂生物表面活性剂的集体表面运动。我们首先表明，群集运动对 rhlA(-)“骗子”的进化具有免疫力。然后，我们证明了铜绿假单胞菌通过代谢谨慎来抵抗欺骗：野生型细胞仅在生物表面活性剂的生产成本和对个体适应性的影响较低时才分泌生物表面活性剂，从而防止不分泌的菌株获得进化优势。代谢谨慎之所以有效，是因为富含碳的生物表面活性剂只有在生长受到另一种生长限制营养物（氮源）限制时才会产生。通过遗传操纵使一种菌株持续产生生物表面活性剂，我们发现群集运动变得容易被欺骗：一个不分泌的菌株会迅速竞争并取代这种必需的合作者。我们认为，代谢谨慎可能首先是作为对欺骗的直接反应而进化的，或者只是为了优化生长，它可以解释许多细菌中大量分泌的维持机制。更广泛地说，审慎的调控是稳定合作的一种机制。
