Thermodynamic constraints on the assembly and diversity of microbial ecosystems are different near to and far from equilibrium.

Thermodynamic constraints on the assembly and diversity of microbial ecosystems are different near to and far from equilibrium.
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DOI:
10.1371/journal.pcbi.1009643
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发表时间:
2021-12
影响因子:
4.3
通讯作者:
Endres RG
Endres RG
中科院分区:
生物学2区
文献类型:
--
作者:
Cook J;Pawar S;Endres RG

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非平衡态热力学长期以来一直是生态学家感兴趣的领域,因为大多数基本的生物过程,如蛋白质合成和呼吸,本质上是消耗能量的。然而,大多数人的兴趣集中在开发粗糙的生态系统级的最大化原则,提供很少的洞察到潜在的机制,导致这种紧急的限制。微生物群落是一个自然的系统,以破译这一机制的基础,因为它们的相互作用的形式,底物消耗,代谢产物的生产,和交叉喂养可以明确地描述在热力学术语。以前的工作已经考虑了热力学约束如何影响物种对之间的竞争,但限制分析这是如何表现在复杂的动力系统。为了解决这一差距,我们开发了一个热力学微生物群落模型与完全可逆的反应动力学,它允许直接考虑自由能耗散。这也允许物种通过产品而不仅仅是底物相互作用,增加了动力学的复杂性,并允许出现更细致的相互作用类型分类。使用这个模型,我们发现,社区的多样性增加与基板不稳定性,因为更大的自由能的可用性允许更快地生成的小生境。因此,在群落建立的时间框架内产生更多的生态位,导致更高的最终物种多样性。我们还发现,允许物种利用接近平衡的反应增加了低自由能制度的多样性。在这样的制度,我们在这里确定两个新的热力学相互作用类型达到可比的传统(竞争和促进)类型的实力,强调热力学在社区动态中发挥的关键作用。我们的研究结果表明,占现实的热力学约束是至关重要的了解现实世界中的微生物群落的动态。由于微生物群落在生物地球化学循环以及动植物健康中的重要作用,人们对微生物群落的兴趣越来越大。虽然我们对单个细胞热力学约束的理解正在迅速提高,但这些约束对复杂微生物群落的影响在理论和经验上仍然很大程度上未被探索。在这里,我们开发了一个新的微生物群落模型,可以直接计算热力学效率和熵产生。我们发现,具有更大的自由能的基板的可用性允许更快的速率的生态位生成,导致更高的最终物种多样性。我们还表明,当自由能的可用性是低的,物种的反应接近热力学平衡的青睐,导致更多样化和有效的社区。除了传统的相互作用类型(竞争和促进),我们的模型揭示了存在两种新的相互作用类型介导的产品,而不是基板。虽然传统的相互作用通常是最强的,新的相互作用类型是显着的自由能可用性低时。我们的研究结果表明,非平衡热力学需要考虑时,研究微生物群落动力学。
Non-equilibrium thermodynamics has long been an area of substantial interest to ecologists because most fundamental biological processes, such as protein synthesis and respiration, are inherently energy-consuming. However, most of this interest has focused on developing coarse ecosystem-level maximisation principles, providing little insight into underlying mechanisms that lead to such emergent constraints. Microbial communities are a natural system to decipher this mechanistic basis because their interactions in the form of substrate consumption, metabolite production, and cross-feeding can be described explicitly in thermodynamic terms. Previous work has considered how thermodynamic constraints impact competition between pairs of species, but restrained from analysing how this manifests in complex dynamical systems. To address this gap, we develop a thermodynamic microbial community model with fully reversible reaction kinetics, which allows direct consideration of free-energy dissipation. This also allows species to interact via products rather than just substrates, increasing the dynamical complexity, and allowing a more nuanced classification of interaction types to emerge. Using this model, we find that community diversity increases with substrate lability, because greater free-energy availability allows for faster generation of niches. Thus, more niches are generated in the time frame of community establishment, leading to higher final species diversity. We also find that allowing species to make use of near-to-equilibrium reactions increases diversity in a low free-energy regime. In such a regime, two new thermodynamic interaction types that we identify here reach comparable strengths to the conventional (competition and facilitation) types, emphasising the key role that thermodynamics plays in community dynamics. Our results suggest that accounting for realistic thermodynamic constraints is vital for understanding the dynamics of real-world microbial communities. There is a growing interest in microbial communities due to their important role in biogeochemical cycling as well as plant and animal health. Although our understanding of thermodynamic constraints on individual cells is rapidly improving, the impact of these constraints on complex microbial communities remains largely unexplored theoretically and empirically. Here, we develop a new microbial community model which allows thermodynamic efficiency and entropy production to be calculated directly. We find that availability of substrates with greater free-energy allows for a faster rate of niche generation, leading to higher final species diversity. We also show that when the free-energy availability is low, species with reactions close to thermodynamic equilibrium are favoured, leading to more diverse and efficient communities. In addition to the conventional interaction types (competition and facilitation), our model reveals the existence of two novel interaction types mediated by products rather than substrates. Though the conventional interactions are generally the strongest, the novel interaction types are significant when free-energy availability is low. Our results suggest that non-equilibrium thermodynamics need to be considered when studying microbial community dynamics.
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