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

合作伙伴选择：宿主如何选择和控制其微生物组？

• 批准号: NE/M015033/1
• 负责人: Matthew Hutchings
• 金额: $ 58.01万
• 依托单位: University of East Anglia
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2015
• 资助国家: 英国
• 起止时间: 2015 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FM015033%2F1
• 关键词: Partner; choice; How; does; host

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.

美洲热带的一群蚂蚁，被称为阿丁蚂蚁，在5000万到6000万年前进化出了农业。这些蚂蚁收集植物材料并将其带回巢穴，在那里它们将其咀嚼并将其喂给一种只能生活在蚂蚁巢穴中的特殊真菌。进化程度最高的昆虫被称为切叶虫，因为它们会从雨林的树冠高处积极地切下树叶，然后把它们带回去作为真菌的食物。作为住房和食物的回报，真菌产生富含脂肪和糖的结构，称为gongylidia，蚂蚁收获作为食物。科学家称这种相互依赖为互利共生，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，最终会消耗花园。蚂蚁还使用抗生素来杀死外来微生物。他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，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互利共生的，因为细菌对抗疾病，作为回报，它们生活在蚂蚁身上，蚂蚁身上的特殊腺体似乎为细菌提供了食物。在NERC之前的资助下，我们已经证明了不同的放线菌生活在蚂蚁身上，并提供了抗生素的混合物，可能是为了减缓入侵真菌花园的疾病的抗生素耐药性的进化。生物学家将生活在宿主生物体上的细菌群落称为微生物组。在蚂蚁的微生物组中，一组被称为假诺卡氏菌的放线菌已经代代相传（垂直传播），并适应了它们的蚂蚁宿主。其他放线菌，大多数属于链霉菌属，似乎每一代都从土壤中重新获得（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，产生寄生虫的细菌，而不是有害或无用的细菌。蚂蚁如何做出正确的伙伴选择？我们已经证明，要入侵一只被假诺卡氏菌覆盖的蚂蚁，另一种细菌菌株必须制造抗生素，这样它才能与假诺卡氏菌争夺一些空间，而且它还必须对假诺卡氏菌制造的抗生素有抗性，这样它才不会被杀死。我们称之为筛选，它导致微生物组由产抗生素和耐药细菌主导，当然，这是蚂蚁所期望的结果，因为它得到了抗生素的混合物。在这个新项目中，我们希望更深层次地了解这个系统，将假诺卡氏菌互利共生菌分开，以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，以及这是否是假诺卡氏菌的私有或公共，即所有细菌均可获得。我们还计划进行实验，以找出这些切叶蚁群中存在的细菌以及它们在个体蚂蚁身上的确切位置。通过这种方式，我们将构建动物宿主的第一个3D微生物组图谱，并将其与最丰富的抗生素图谱重叠。利用蚂蚁来研究和模拟这些微生物群的优势在于，它们易于保存，而且它们的微生物群在外部，这意味着我们可以用它们做实验。这给了我们希望，我们可以制定出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。

项目成果

Genome Analysis of Two Pseudonocardia Phylotypes Associated with Acromyrmex Leafcutter Ants Reveals Their Biosynthetic Potential.

• DOI: 10.3389/fmicb.2016.02073
• 发表时间: 2016
• 期刊: Frontiers in microbiology
• 影响因子: 5.2
• 作者: Holmes NA;Innocent TM;Heine D;Bassam MA;Worsley SF;Trottmann F;Patrick EH;Yu DW;Murrell JC;Schiøtt M;Wilkinson B;Boomsma JJ;Hutchings MI
• 通讯作者: Hutchings MI

Chemical warfare between fungus-growing ants and their pathogens.

• DOI: 10.1016/j.cbpa.2020.08.001
• 发表时间: 2020-12
• 期刊: Current opinion in chemical biology
• 影响因子: 7.8
• 作者: Batey SFD;Greco C;Hutchings MI;Wilkinson B
• 通讯作者: Wilkinson B

The MtrAB two-component system controls antibiotic production in Streptomyces coelicolor A3(2).

• DOI: 10.1099/mic.0.000524
• 发表时间: 2017-10
• 期刊: Microbiology (Reading, England)
• 作者: Som NF;Heine D;Holmes N;Knowles F;Chandra G;Seipke RF;Hoskisson PA;Wilkinson B;Hutchings MI
• 通讯作者: Hutchings MI

Formicamycins, antibacterial polyketides produced by Streptomyces formicae isolated from African Tetraponera plant-ants.

• DOI: 10.1039/c6sc04265a
• 发表时间: 2017-04-01
• 期刊: Chemical science
• 影响因子: 8.4
• 作者: Qin Z;Munnoch JT;Devine R;Holmes NA;Seipke RF;Wilkinson KA;Wilkinson B;Hutchings MI
• 通讯作者: Hutchings MI

Chemical warfare between leafcutter ant symbionts and a co-evolved pathogen.

• DOI: 10.1038/s41467-018-04520-1
• 发表时间: 2018-06-07
• 期刊: Nature communications
• 影响因子: 16.6
• 作者: Heine D;Holmes NA;Worsley SF;Santos ACA;Innocent TM;Scherlach K;Patrick EH;Yu DW;Murrell JC;Vieria PC;Boomsma JJ;Hertweck C;Hutchings MI;Wilkinson B
• 通讯作者: Wilkinson B