BBSRC-NSF/BIO - The impact of public versus private metabolism on the stability of microbial communities within natural hosts

BBSRC-NSF/BIO - 公共代谢与私人代谢对自然宿主内微生物群落稳定性的影响

• 批准号: BB/T015985/1
• 负责人: Ivana Gudelj
• 金额: $ 57.36万
• 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: 2020
• 资助国家: 英国
• 起止时间: 2020 至 无数据
• 项目状态: 未结题
• 来源: https://gtr.ukri.org/projects?ref=BB%2FT015985%2F1
• 关键词: BBSRC; NSF; BIO; impact; public

Why do microorganisms engage in cooperative nutrient consumption that is open to exploitation when an exploitation-free alternative is available? Our proposal will answer this fundamental yet unanswered question through a combination of synthetic biology, mathematical modelling and in vivo microbial community experiments. Microorganisms play crucial roles in ecosystem functioning and the health of macro organisms. They form beneficial relationships with multicellular organisms, in environments ranging from animal guts to soil, and can be exploited to degrade industrial waste or produce useful chemicals. But they can also cause devastating damage by destroying our food sources and eliminating key plant species, thus preventing the absorption of hundreds of megatonnes of CO2. Microorganisms do not exist in isolation, instead they form intricate communities of diverse strains and species where individuals participate in complex cooperative and competitive interactions. However, we lack a comprehensive understanding of how these interactions alter the function and stability of the community. This is crucial for predicting the evolution of microbial strategies that promote survival and growth in natural environments.To survive and thrive, microorganisms must obtain nutrients from their environment and cooperative and competitive actions are key to the way that microbes feed. A common strategy to obtain nutrients involves secreting metabolic products into the external, "public" environment to break down or capture resources, before they are taken up into the cell. The metabolic products are considered to be cooperative public goods as they are generated externally and so benefit other cells in the shared environment. This seemingly successful strategy, termed "public metabolism", is used by a wide range of microbial species that inhabit diverse habitats, yet it has two obvious drawbacks. First, the public goods can easily be lost into the environment before they are successfully taken up by the cell that generated them. Second, the public-goods can be exploited by microbes that "cheat" by not contributing to their production but still reap the rewards. These shortcomings can threaten the success of public metabolism and the stability and functioning of microbial communities. Curiously, an exploitation-free strategy exists whereby microbes can secure nutrients by taking them directly into the cell, with digestion taking place "privately" inside the cell, instead of "publicly" in the environment. Yet despite this failsafe alternative, many microbes still feed by public metabolism. Our project will determine why this is the case and what benefits public metabolism provides.Based on preliminary data we hypothesise that microbial feeding strategies involving either public or private metabolism represent two opposing approaches to survival, the success of which is environment-dependent. In particular, we hypothesise that sufficiently spatially structured environments will limit exploitation of public-metabolisers thus favouring them over private-metabolisers.To test this, we have generated two well-defined and tractable synthetic systems involving the environmental yeast Saccharomyces cerevisiae and the plant pathogen Magnaporthe oryzae. These communities will be used to experimentally probe the fitness of different metabolic strategies in their natural environments and assess community stability and function. In parallel, we will develop dynamic, spatially explicit, genome-scale mathematical models to generate mechanistic understanding of how metabolic interactions and the degree of spatial structure support community stability. This will enable us to extrapolate general principles from the system-specific observation and to develop a classification of different types of biotic (e.g. host-pathogen and microbe-microbe) and abiotic (e.g. spatial structure) conditions that favour cooperative metabolism.

当有一种无开采的替代品可用时，微生物为什么要进行可供开采的合作养分消耗？我们的建议将通过结合合成生物学、数学建模和体内微生物群落实验来回答这个基本但尚未回答的问题。微生物在生态系统的功能和大型生物的健康中起着至关重要的作用。在从动物内脏到土壤的各种环境中，它们与多细胞生物体形成了有益的关系，并可被利用来降解工业废物或生产有用的化学品。但它们也可能造成毁灭性的破坏，破坏我们的食物来源，消灭关键植物物种，从而阻止数亿吨二氧化碳的吸收。微生物并不是孤立存在的，而是由不同的菌株和物种组成复杂的群落，在这些群落中，个体参与复杂的合作和竞争相互作用。然而，对于这些互动如何改变社区的功能和稳定，我们缺乏全面的了解。这对于预测促进自然环境中生存和生长的微生物策略的演变至关重要。为了生存和茁壮成长，微生物必须从环境中获得营养，而合作和竞争行动是微生物觅食方式的关键。获取营养的一种常见策略是，在代谢产物进入细胞之前，将代谢产物分泌到外部的“公共”环境中，以分解或捕获资源。代谢产物被认为是合作的公共产品，因为它们是从外部产生的，因此有利于共享环境中的其他细胞。这一看似成功的策略被称为“公共新陈代谢”，被生活在不同栖息地的各种微生物物种所使用，但它有两个明显的缺点。首先，在公共产品被产生它们的细胞成功吸收之前，它们很容易就会丢失到环境中。其次，公共产品可能会被微生物利用，这些微生物通过不贡献它们的生产来“欺骗”，但仍然获得了回报。这些缺陷可能会威胁到公共新陈代谢的成功以及微生物群落的稳定和功能。奇怪的是，存在一种无需开发的策略，微生物可以通过将营养物质直接带入细胞来确保营养，消化过程在细胞内“私下”进行，而不是在环境中“公开”进行。然而，尽管有这种故障保险的替代方案，许多微生物仍然以公共新陈代谢为生。我们的项目将确定为什么会这样，以及公共新陈代谢提供了什么好处。基于初步数据，我们假设，涉及公共新陈代谢或私人新陈代谢的微生物喂养策略代表了两种截然相反的生存方式，其成功与否取决于环境。特别是，我们假设空间结构充分的环境将限制公共代谢物的开发，从而有利于公共代谢物而不是私人代谢物。为了测试这一点，我们生成了两个定义良好且易于处理的合成系统，涉及环境酵母酿酒酵母和植物病原菌稻瘟病菌。这些群落将被用来实验性地探索不同新陈代谢策略在其自然环境中的适用性，并评估群落的稳定性和功能。同时，我们将开发动态的、空间上明确的、基因组规模的数学模型，以产生对新陈代谢相互作用和空间结构程度如何支持群落稳定性的机械性理解。这将使我们能够从特定系统的观察中推断出一般原则，并对有利于合作新陈代谢的不同类型的生物(例如寄主-病原体和微生物-微生物)和非生物(例如空间结构)条件进行分类。

项目成果

Predicting microbial growth dynamics in response to nutrient availability.

• DOI: 10.1371/journal.pcbi.1008817
• 发表时间: 2021-03
• 期刊: PLoS computational biology
• 影响因子: 4.3
• 作者: Nev OA;Lindsay RJ;Jepson A;Butt L;Beardmore RE;Gudelj I
• 通讯作者: Gudelj I

Would that it were so simple: Interactions between multiple traits undermine classical single-trait-based predictions of microbial community function and evolution.

• DOI: 10.1111/ele.13861
• 发表时间: 2021-08
• 期刊: Ecology letters
• 影响因子: 8.8
• 作者: Richard J. Lindsay;Alys Jepson;Lisa Butt;Philippa J. Holder;Bogna J. Smug;I. Gudelj