High-order interactions distort the functional landscape of microbial consortia

Understanding the link between community composition and function is a major challenge in microbial population biology, with implications for the management of natural microbiomes and the design of synthetic consortia. Specifically, it is poorly understood whether community functions can be quantitatively predicted from traits of species in monoculture. Inspired by the study of complex genetic interactions, we have examined how the amylolytic rate of combinatorial assemblages of six starch-degrading soil bacteria depend on the separate functional contributions from each species and their interactions. Filtering our results through the theory of biochemical kinetics, we show that this simple function is additive in the absence of interactions among community members. For about half of the combinatorially assembled consortia, the amylolytic function is dominated by pairwise and higher-order interactions. For the other half, the function is additive despite the presence of strong competitive interactions. We explain the mechanistic basis of these findings and propose a quantitative framework that allows us to separate the effect of behavioral and population dynamics interactions. Our results suggest that the functional robustness of a consortium to pairwise and higher-order interactions critically affects our ability to predict and bottom-up engineer ecosystem function in complex communities.解析群落组成与功能间的关联，是微生物种群生物学领域的核心挑战之一，其研究结果对自然微生物组（microbiome）的管护以及合成微生物群落（synthetic consortium）的设计构建具有重要参考价值。具体而言，目前学界尚未明确能否通过单培养（monoculture）物种的性状，对群落功能实现定量预测。受复杂遗传互作研究的启发，本研究针对6株淀粉降解土壤细菌的组合群落，探究了其淀粉水解速率如何受各物种独立功能贡献及其相互作用的影响。借助生化动力学理论对研究结果进行分析后，我们发现：当群落成员间无相互作用时，该简单功能（淀粉水解速率）呈现加和性特征。在约半数组合构建的合成群落中，淀粉水解功能由成对互作与高阶互作主导；而剩余半数群落即便存在强烈的竞争互作，其功能仍呈加和性。本研究阐明了上述发现的机制基础，并提出一套定量分析框架，可用于区分行为互作与种群动态互作的效应。研究结果表明，合成群落对成对及高阶互作的功能鲁棒性（robustness），将显著影响我们对复杂群落进行功能预测与自下而上工程化构建的能力。