Department of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag), 8600, Dübendorf, Switzerland.
Department of Environmental Systems Science, ETH Zürich, 8092, Zürich, Switzerland.
ISME J. 2022 May;16(5):1453-1463. doi: 10.1038/s41396-022-01189-9. Epub 2022 Jan 25.
Spatial self-organization is a hallmark of surface-associated microbial communities that is governed by local environmental conditions and further modified by interspecific interactions. Here, we hypothesize that spatial patterns of microbial cell-types can stabilize the composition of cross-feeding microbial communities under fluctuating environmental conditions. We tested this hypothesis by studying the growth and spatial self-organization of microbial co-cultures consisting of two metabolically interacting strains of the bacterium Pseudomonas stutzeri. We inoculated the co-cultures onto agar surfaces and allowed them to expand (i.e. range expansion) while fluctuating environmental conditions that alter the dependency between the two strains. We alternated between anoxic conditions that induce a mutualistic interaction and oxic conditions that induce a competitive interaction. We observed co-occurrence of both strains in rare and highly localized clusters (referred to as "spatial jackpot events") that persist during environmental fluctuations. To resolve the underlying mechanisms for the emergence of spatial jackpot events, we used a mechanistic agent-based mathematical model that resolves growth and dispersal at the scale relevant to individual cells. While co-culture composition varied with the strength of the mutualistic interaction and across environmental fluctuations, the model provides insights into the formation of spatially resolved substrate landscapes with localized niches that support the co-occurrence of the two strains and secure co-culture function. This study highlights that in addition to spatial patterns that emerge in response to environmental fluctuations, localized spatial jackpot events ensure persistence of strains across dynamic conditions.
空间自组织是表面相关微生物群落的一个标志，受局部环境条件控制，并进一步受种间相互作用的影响。在这里，我们假设微生物细胞类型的空间模式可以在环境条件波动的情况下稳定交叉喂养微生物群落的组成。我们通过研究由两种代谢相互作用的假单胞菌组成的微生物共培养物的生长和空间自组织来检验这一假设。我们将共培养物接种到琼脂表面上，并允许它们在改变两种菌株之间依赖性的环境条件下扩展（即范围扩展）。我们在缺氧条件下交替进行，诱导互利相互作用，在有氧条件下诱导竞争相互作用。我们观察到两种菌株在罕见的和高度本地化的簇（称为“空间 jackpot 事件”）中共存，这些事件在环境波动期间持续存在。为了解决空间 jackpot 事件出现的潜在机制，我们使用了一种机制性的基于主体的数学模型，该模型可解决与单个细胞相关的规模上的生长和扩散问题。虽然共培养物组成随互利相互作用的强度和环境波动而变化，但该模型提供了对具有局部小生境的空间分辨底物景观形成的深入了解，这些小生境支持两种菌株的共存，并确保共培养物的功能。这项研究强调，除了响应环境波动而出现的空间模式外，局部空间 jackpot 事件还确保了菌株在动态条件下的持续存在。
