Sex and Death: testing the evolutionary benefit of recombination using a bacterium and bacteriophage model

性与死亡：使用细菌和噬菌体模型测试重组的进化益处

• 批准号: NE/K000926/1
• 负责人: Michiel Vos
• 金额: $ 10.18万
• 依托单位: UNIVERSITY OF EXETER
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2013
• 资助国家: 英国
• 起止时间: 2013 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FK000926%2F1
• 关键词: Sex; Death; testing; evolutionary; benefit

General SummaryBackgroundAlthough bacteria reproduce through binary fission, they are not purely clonal. On occasion, they are capable of taking up DNA from the environment derived from other bacterial cells and recombine it with their own genetic material. This process is termed transformation. Just as in plant and animal sex, this shuffling of DNA increases the genetic variation in the population. The process of natural selection needs such genetic variation in the population to be able to select the fittest individuals. Populations of organisms that engage in sex (or more generally recombination) could thus be assumed to adapt more quickly to their environment. However, recombination is only favoured when the environment is ever-changing. If not, recombination would eventually disassemble the fittest combinations of DNA it had created. The strongest candidate for both strong and continuously fluctuating selection is that of parasite attack. Parasites and hosts are locked in a continuing arms race: hosts develop resistance against their parasites, and parasites evolve to overcome this resistance and so on and so forth. This scenario is named 'the Red Queen Hypothesis' after Lewis Carroll's book Through the Looking-Glass, where the Red Queen tells Alice: 'It takes all the running you can do, to keep in the same place'. AimThe Red Queen Hypothesis is especially likely to be applicable to bacteria for two reasons. First, bacteria are frequently attacked by deadly viruses (bacteriophages), exerting very strong selection for novel resistance. Second, bacterial recombination is 'cheaper' than that of many plants and animals. For instance, bacteria do not rely on sex for reproduction and could resort to it only when needed. Although a lot of theory has been developed, experimental tests of the Red Queen Hypothesis are rare. Here, we propose to experimentally coevolve the aquatic bacterium Aeromonas, known to frequently recombine, with phage. The quality of free DNA available for transformation will be experimentally manipulated. This will allow us to for the first time quantify whether 'bacterial sex' can aid adaptation to parasitic viruses. Transformation results in the reshuffling of all polymorphisms in the population, not only those associated with resistance to phage. We therefore will also include a temperature treatment where high, stressful temperature requires additional adaptation with an expected greater potential benefit of recombination. Applications and BenefitsBacteria and phage are an ideal model system to test the Red Queen Hypothesis, but are also of great importance to human health and the economy. Various Aeromonas species are opportunistic pathogens causing a wide range of infections. Aeromonas is a pathogen on the rise and has been found to be the most common cause of soft tissue and skin infections in a study on survivors of the 2004 tsunami in Asia. Bacteriophages are important agents of bacterial mortality. With increasing levels of bacterial resistance to antibiotics, phage therapy has received renewed interest as an alternative strategy to prevent and fight infection by using phages as 'evolving antibiotics'. Importantly, this project will test whether coevolution with phage selects for increased transformation. Phage therapy designed to limit the negative impact of pathogenic bacteria thus could actually result in the increased capability of bacteria to evolve virulence or antibiotic resistance through transformation. Finding any increased benefit of recombination at higher temperature could have important implications for evolutionary change in response to climate change. This will be the first study explicitly linking phage coevolution and transformation, two main evolutionary forces in microbiology, and is bound to yield exciting new insights with special relevance to fighting an opportunistic pathogen.

背景虽然细菌通过二分裂繁殖，但它们不是纯克隆的。有时，它们能够从环境中吸收来自其他细菌细胞的DNA，并将其与自己的遗传物质重组。这个过程被称为转化。就像植物和动物的性别一样，这种DNA的改组增加了种群的遗传变异。自然选择的过程需要种群中的这种遗传变异，以便能够选择最适合的个体。因此，可以假设进行有性繁殖（或者更一般地说，进行重组）的生物种群能够更快地适应环境。然而，只有在环境不断变化的情况下，重组才是有利的。如果没有，重组最终会分解它所创造的最合适的DNA组合。强选择和连续波动选择的最强候选者是寄生虫攻击。寄生虫和宿主被锁定在一个持续的军备竞赛中：宿主对它们的寄生虫产生抵抗力，寄生虫进化以克服这种抵抗力，等等。这种情况被命名为“红皇后假说”，这是根据刘易斯卡罗尔的《镜中奇遇记》一书命名的。书中红皇后告诉爱丽丝：“你要尽全力奔跑，才能保持在同一个地方。”红皇后假说特别可能适用于细菌，原因有二。首先，细菌经常受到致命病毒（噬菌体）的攻击，对新的抗性施加非常强的选择。第二，细菌重组比许多动植物重组“便宜”。例如，细菌不依赖性繁殖，只有在需要的时候才能求助于性。虽然已经发展了很多理论，但对红皇后假说的实验测试很少。在这里，我们建议实验共同进化的水生细菌气单胞菌，已知经常重组，与噬菌体。将通过实验操作可用于转化的游离DNA的质量。这将使我们能够首次量化“细菌性别”是否有助于适应寄生病毒。转化导致种群中所有多态性的重新洗牌，而不仅仅是那些与噬菌体抗性相关的多态性。因此，我们还将包括一个温度处理，其中高，压力温度需要额外的适应与预期的更大的重组潜在效益。细菌和噬菌体是测试红皇后假说的理想模型系统，但对人类健康和经济也非常重要。各种气单胞菌属物种是引起广泛感染的条件致病菌。气单胞菌是一种正在上升的病原体，在一项对2004年亚洲海啸幸存者的研究中发现，气单胞菌是软组织和皮肤感染的最常见原因。噬菌体是细菌死亡的重要因子。随着细菌对抗生素耐药性水平的提高，噬菌体疗法作为一种替代策略，通过使用噬菌体“进化的抗生素”来预防和对抗感染，已经重新受到关注。重要的是，该项目将测试与噬菌体的共同进化是否会选择增加转化。因此，旨在限制致病菌负面影响的噬菌体疗法实际上可能导致细菌通过转化进化毒力或抗生素抗性的能力增加。发现在更高温度下重组的任何增加的益处可能对应对气候变化的进化变化具有重要意义。这将是第一项明确将噬菌体协同进化和转化（微生物学中的两种主要进化力量）联系起来的研究，并且必将产生令人兴奋的新见解，与对抗机会病原体特别相关。

项目成果

No effect of natural transformation on the evolution of resistance to bacteriophages in the Acinetobacter baylyi model system.

• DOI: 10.1038/srep37144
• 发表时间: 2016-11-21
• 期刊: Scientific reports
• 影响因子: 4.6
• 作者: McLeman A;Sierocinski P;Hesse E;Buckling A;Perron G;Hülter N;Johnsen PJ;Vos M
• 通讯作者: Vos M

A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus.

• DOI: 10.1038/ismej.2016.34
• 发表时间: 2016-10
• 期刊: The ISME journal

Triclosan Alters Microbial Communities in Freshwater Microcosms

• DOI: 10.3390/w11050961
• 发表时间: 2019-05-01
• 期刊: WATER
• 影响因子: 3.4
• 作者: Clarke, Alexandra;Azulai, Daniella;Perron, Gabriel G.
• 通讯作者: Perron, Gabriel G.