Finn Damien Robert, App Mario, Hertzog Lionel, Tebbe Christoph C
Thünen Institut für Biodiversität, Johann Heinrich von Thünen Institut, Braunschweig, Germany.
Front Microbiol. 2022 Sep 15;13:969784. doi: 10.3389/fmicb.2022.969784. eCollection 2022.
The Black Queen hypothesis describes the evolutionary strategy to lose costly functions in favour of improving growth efficiency. This results in mutants (cheaters) becoming obligately dependent upon a provider (black queen) to produce a necessary resource. Previous analyses demonstrate black queens and cheaters reach a state of equilibrium in pair-wise systems. However, in complex communities, accumulation of cheaters likely poses a serious burden on shared resources. This should result in a Tragedy of the Commons (ToC), whereby over-utilisation of public resources risks making them growth-limiting. With a collection of differential equations, microbial communities composed of twenty prokaryote 'species' either from rhizosphere, characterised by abundant carbon and energy sources, or bulk soil, with limited carbon and energy supply, were simulated. Functional trait groups differed based on combinations of cellulase and amino acid production, growth and resource uptake. Randomly generated communities were thus composed of species that acted as cellulolytic prototrophic black queens, groups that were either cellulolytic or prototrophic, or non-cellulolytic auxotrophic cheaters. Groups could evolve to lose functions over time. Biomass production and biodiversity were tracked in 8,000 Monte Carlo simulations over 500 generations. Bulk soil favoured oligotrophic co-operative communities where biodiversity was positively associated with growth. Rhizosphere favoured copiotrophic cheaters. The most successful functional group across both environments was neither black queens nor cheaters, but those that balanced providing an essential growth-limiting function at a relatively low maintenance cost. Accumulation of loss of function mutants in bulk soil risked resulting in loss of cumulative growth by ToC, while cumulative growth increased in the rhizosphere. In the bulk soil, oligotrophic adaptations assisted species in avoiding extinction. This demonstrated that loss of function by mutation is a successful evolutionary strategy in host-associated and/or resource-rich environments, but poses a risk to communities that must co-operate with each other for mutual co-existence. It was concluded that microbial communities must follow different evolutionary and community assembly strategies in bulk soil versus rhizosphere, with bulk soil communities more dependent on traits that promote co-operative interactions between microbial species.
黑皇后假说描述了一种进化策略，即通过舍弃代价高昂的功能来提高生长效率。这导致突变体（作弊者）必须依赖提供者（黑皇后）来产生一种必要资源。先前的分析表明，在两两系统中，黑皇后和作弊者会达到一种平衡状态。然而，在复杂群落中，作弊者的积累可能会给共享资源带来沉重负担。这应该会导致公地悲剧（ToC），即公共资源的过度利用可能会使其成为生长限制因素。通过一组微分方程，模拟了由20种原核“物种”组成的微生物群落，这些“物种”要么来自根际，其特点是碳源和能源丰富，要么来自土体土壤，碳源和能源供应有限。功能性状组根据纤维素酶和氨基酸产生、生长和资源摄取的组合而有所不同。随机生成的群落因此由作为纤维素分解原养型黑皇后的物种、纤维素分解或原养型的群体，或非纤维素分解营养缺陷型作弊者组成。随着时间的推移，群体可能会进化而失去功能。在500代的8000次蒙特卡洛模拟中跟踪了生物量生产和生物多样性。土体土壤有利于贫营养合作群落，其中生物多样性与生长呈正相关。根际有利于富营养作弊者。在这两种环境中最成功的功能组既不是黑皇后也不是作弊者，而是那些以相对较低的维持成本平衡提供基本生长限制功能的组。土体土壤中功能丧失突变体的积累有可能导致因公地悲剧而使累积生长丧失，而根际中的累积生长则增加。在土体土壤中，贫营养适应有助于物种避免灭绝。这表明，通过突变导致的功能丧失在宿主相关和/或资源丰富的环境中是一种成功的进化策略，但对必须相互合作以实现共存的群落构成风险。得出的结论是，微生物群落在土体土壤和根际必须遵循不同的进化和群落组装策略，土体土壤群落更依赖于促进微生物物种间合作相互作用的性状。
