Department of Biology, Indiana University, Bloomington, Indiana, USA.
Department of Biology, Indiana University, Bloomington, Indiana, USA
mBio. 2017 Nov 28;8(6):e01620-17. doi: 10.1128/mBio.01620-17.
Many mutualistic microbial relationships are based on nutrient cross-feeding. Traditionally, cross-feeding is viewed as being unidirectional, from the producer to the recipient. This is likely true when a producer's waste, such as a fermentation product, has value only for a recipient. However, in some cases the cross-fed nutrient holds value for both the producer and the recipient. In such cases, there is potential for nutrient reacquisition by producer cells in a population, leading to competition against recipients. Here, we investigated the consequences of interpartner competition for cross-fed nutrients on mutualism dynamics by using an anaerobic coculture pairing fermentative and phototrophic In this coculture, excretes waste organic acids that provide a carbon source for In return, cross-feeds ammonium (NH), a compound that both species value. To explore the potential for interpartner competition, we first used a kinetic model to simulate cocultures with varied affinities for NH in each species. The model predicted that interpartner competition for NH could profoundly impact population dynamics. We then experimentally tested the predictions by culturing mutants lacking NH transporters in both NH competition assays and mutualistic cocultures. Both theoretical and experimental results indicated that the recipient must have a competitive advantage in acquiring cross-fed NH to sustain the mutualism. This recipient-biased competitive advantage is predicted to be crucial, particularly when the communally valuable nutrient is generated intracellularly. Thus, the very metabolites that form the basis for mutualistic cross-feeding can also be subject to competition between mutualistic partners. Mutualistic relationships, particularly those based on nutrient cross-feeding, promote stability of diverse ecosystems and drive global biogeochemical cycles. Cross-fed nutrients within these systems can be either waste products valued by only one partner or nutrients valued by both partners. Here, we explored how interpartner competition for a communally valuable cross-fed nutrient impacts mutualism dynamics. We discovered that mutualism stability necessitates that the recipient have a competitive advantage against the producer in obtaining the cross-fed nutrient, provided that the nutrient is generated intracellularly. We propose that the requirement for recipient-biased competition is a general rule for mutualistic coexistence based on the transfer of intracellularly generated, communally valuable resources.
许多互利共生的微生物关系是基于营养物质的交叉喂养。传统上，交叉喂养被认为是单向的，从生产者到接受者。当生产者的废物（如发酵产物）对接受者只有价值时，这种情况很可能是正确的。然而，在某些情况下，交叉喂养的营养物质对生产者和接受者都有价值。在这种情况下，种群中的生产者细胞有可能重新获取营养物质，从而与接受者竞争。在这里，我们通过使用一种厌氧共培养物对发酵和光合微生物进行配对，研究了交叉喂养的营养物质的伙伴间竞争对互利共生动态的影响。在这种共培养物中， 分泌出的有机废酸为 提供了碳源。作为回报， 交叉喂养 铵（NH），这是两种生物都看重的化合物。为了探索伙伴间竞争的可能性，我们首先使用动力学模型模拟了每个物种中对 NH 亲和力不同的共培养物。该模型预测，NH 的伙伴间竞争可能会对种群动态产生深远影响。然后，我们通过在 NH 竞争测定和互利共生共培养物中培养缺乏 NH 转运蛋白的突变体来实验验证预测。理论和实验结果都表明，接受者必须在获取交叉喂养的 NH 方面具有竞争优势，以维持互利共生关系。这种有利于接受者的竞争优势预计是至关重要的，特别是当共同有价值的营养物质在细胞内产生时。因此，形成互利共生交叉喂养基础的代谢物本身也可能成为互利共生伙伴之间竞争的对象。互利共生关系，特别是基于营养物质交叉喂养的关系，促进了多样化生态系统的稳定性，并推动了全球生物地球化学循环。这些系统中的交叉喂养营养物质可以是只有一个伙伴重视的废物产物，也可以是两个伙伴都重视的营养物质。在这里，我们探讨了伙伴间对共同有价值的交叉喂养营养物质的竞争如何影响互利共生动态。我们发现，只要营养物质在细胞内产生，互利共生的稳定性就需要接受者在获取交叉喂养营养物质方面相对于生产者具有竞争优势。我们提出，基于细胞内产生的、共同有价值的资源的转移，对接受者有利的竞争是互利共生共存的一般规则。
