Partner choice: How does a host select and control its microbiome?

美洲热带地区的一群蚂蚁，被称为蚂蚁，在五六千万年前进化出了农业。这些蚂蚁收集植物材料并将其带回巢穴，在那里它们咀嚼它并将其喂给一种特殊的真菌，这种真菌只能生活在蚁巢中。进化程度最高的蜜蜂被称为“切叶者”，因为它们会主动从雨林冠层高处砍下树叶，并把它们带回作为真菌的食物。作为住房和食物的回报，这种真菌会产生富含脂肪和糖的结构，被称为蚁体，蚂蚁可以将其作为食物收获。科学家称这种相互依赖为互惠互利，因为蚂蚁和真菌相互受益。蚂蚁通过清除不需要的微生物（真菌和细菌）来保护它们宝贵的真菌花园，如果不加以控制，这些微生物最终会吞噬整个花园。蚂蚁还会使用抗生素来杀死外来微生物。它们从另一种共生菌那里获得抗生素，这是一种特殊的丝状细菌，被称为放线菌，它以制造多种抗生素而闻名（在生物学家中）。放线菌与蚂蚁和真菌花园是共生的，因为细菌与疾病作斗争，作为回报，它们生活在蚂蚁的身体上，而蚂蚁的身体上似乎有专门的腺体为细菌提供食物。在之前NERC的资助下，我们已经证明了不同的放线菌细菌生活在蚂蚁身上，并提供抗生素的混合物，可能是为了减缓入侵真菌花园的疾病对抗生素耐药性的进化。生物学家把寄生在宿主体内的细菌群落称为微生物群。在蚁群微生物组中，一组放线菌，被称为伪心放线菌，已经代代相传（垂直传播），并且已经适应了它们的蚂蚁宿主。其他放线菌，主要是链霉菌，似乎每一代都从土壤中获得新的（水平传播）。这是令人惊讶的，因为土壤中充满了细菌，其中大多数不是链霉菌，但不知何故，蚂蚁能够选择性地从环境中吸收有用的、产生抗生素的细菌，而不是有害的或无用的细菌。蚂蚁如何做出正确的伴侣选择？我们已经证明，要入侵一只被伪心菌覆盖的蚂蚁，另一种细菌必须产生抗生素，这样它才能与伪心菌争夺一些空间，它还必须对伪心菌产生的抗生素产生抗药性，这样它才不会被杀死。我们称之为筛选，它会产生一个由产生抗生素和耐药细菌主导的微生物群，当然，这是蚂蚁想要的结果，因为它得到了使用抗生素的混合物。在这个新项目中，我们想要在更深层次上了解这个系统，分解假心菌共生菌，了解它们产生的抗生素以及它们如何影响“伴侣选择”，并测试蚂蚁是否真的为细菌提供食物，这是假心菌的私人食物还是公共食物，也就是说，所有细菌都可以获得。我们还计划进行实验，以找出这些切叶蚁表皮上究竟存在哪些细菌，以及它们在单个蚂蚁身上的确切位置。通过这种方式，我们将建立动物宿主的第一个3D微生物组图，并将其覆盖在最丰富的抗生素地图上。用蚂蚁来研究和模拟这些微生物群的好处是，它们很容易保存，它们的微生物群在外面，这意味着我们可以用它做实验。这给我们带来了希望，我们可以制定出指导如何在自由生活的海洋和陆地系统（包括所有陆地植物）中创建和管理保护性微生物群的一般原则。

A group of ants in tropical America, known as the attines, evolved agriculture 50-60 million years ago. These ants collect plant material and take it back to their nests, where they chew it up and feed it to a special fungus that is only able to live in attine ant nests. The most highly evolved attines are known as leafcutters because they actively cut leaves from high up in the rainforest canopy and carry them back as food for their fungus. In return for housing and food, the fungus produces fat- and sugar-rich structures, called gongylidia that the ants harvest as food. Scientists call this co-dependence a mutualism because the ants and the fungus mutually benefit each other. The ants protect their valuable fungal gardens by weeding out unwanted microbes (fungi and bacteria), which, if not controlled, would eventually consume the garden. The ants also apply antibiotics to kill the foreign microbes. They get the antibiotics from another mutualist, a special set of filamentous bacteria, called actinomycetes, which are famous (amongst biologists) for making many kinds of antibiotics. The actinomycetes are mutualists with the ant and the fungus garden, because the bacteria fight disease, and in return, live on the ant bodies, where specialised glands appear to feed the bacteria.With previous NERC funding we have shown that different actinomycete bacteria live on the ants and provide a mixture of antibiotics, probably to slow down the evolution of antibiotic resistance in the diseases that invade the fungus gardens. Biologists call the bacterial communities that live on a host organism its microbiome. In the attine microbiome, one group of actinomycetes, known as Pseudonocardia, have been handed down over generations (vertically transmitted), and have adapted to their ant hosts. Other actinomycetes, mostly in a group called Streptomyces, appear to be acquired anew from the soil in each generation (horizontal transmission). This is surprising, because the soil is full of bacteria, most of which are not Streptomyces, but somehow the ant is able to selectively take up useful, antibiotic-producing bacteria from their environment, and not harmful or useless bacteria. How does the ant make the right Partner Choice? We have shown that to invade an ant covered in Pseudonocardia another bacterial strain must make antibiotics so it can fight the Pseudonocardia for some space and it must also be resistant to antibiotics made by the Pseudonocardia so it doesn't get killed. We call this SCREENING and it results in a microbiome dominated by antibiotic-producing and -resistant bacteria, which, of course, is the desired outcome for the ant because it gets a mixture of antibiotics to use. In this new project we want to understand this system at an even deeper level, taking apart both the Pseudonocardia mutualists to understand the antibiotics they produce and how they influence 'Partner Choice' and to test whether the ants really do provide food to the bacteria and whether this is private to Pseudonocardia or public, that is, available to all bacteria. We also plan experiments to find out exactly which bacteria are present on these leafcutter ant cuticles and exactly where they are on individual ants. In this way we will build the first 3D microbiome maps of an animal host and overlay it with maps of the most abundantly produced antibiotics. The advantage of using attine ants to study and model these microbiomes is that they are easy to keep and their microbiome is on the outside, which means we can do experiments with it. This gives us hope that we can work out general principles governing how to create and manage protective microbiomes in free-living marine and terrestrial systems, including all land plants.