Ninzatti Léa, Sana Thibault G, Acar Tessa, Moreau Sandra, Jardinaud Marie-Françoise, Marti Guillaume, Coen Olivier, Carlier Aurelien L
Laboratoire des Interactions Plantes-Microbes-Environnement (LIPME), Université de Toulouse, INRAE, CNRS, Castanet-Tolosan F-31326, France.
Université de Bordeaux, Pessac F-33600, France.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf177.
Some plants engage in permanent, vertically transmitted symbioses with bacteria. Often, these bacteria are hosted extracellularly within structures on the leaves, where they produce specialized bioactive metabolites that benefit their host. These associations are highly specific, with one plant species associating with a single bacterial species, but little is known about how these symbioses originate and how specificity is maintained. In this study, we show that the symbiotic association between a wild yam and a bacterium can be manipulated experimentally and that bacteria-free plants are open to colonization by environmental bacteria. Through metabolic profiling, we show that the endophytic niche is rich in organic acids and intermediates of the tricarboxylic acid cycle cycle. Environmental bacteria capable of utilizing these acids, such as the soil bacterium Pseudomonas putida, readily colonize aposymbiotic plants. However, successful colonization is contingent upon the absence of the vertically transmitted symbiont or the impairment of its type VI secretion system. Unexpectedly for a vertically transmitted symbiosis, these findings suggest that microbe-microbe interactions, including antagonism, may play a crucial role in maintaining the specificity of an association. However, low transmission rates of synthetic symbionts provide evidence that transmission barriers or bottlenecks may still occur, further enforcing partner fidelity. Together, these results highlight the complexity of mechanisms underlying mutualistic associations, and provide insights into the evolution of bacterial leaf symbiosis.
一些植物与细菌形成了永久性的、垂直传播的共生关系。通常，这些细菌在叶片上的结构中细胞外生存，在那里它们产生有益于宿主的特殊生物活性代谢产物。这些共生关系具有高度特异性，一种植物物种与单一细菌物种相关联，但对于这些共生关系如何起源以及特异性如何维持，人们知之甚少。在本研究中，我们表明野生山药与一种细菌之间的共生关系可以通过实验进行操控，并且无菌植物容易被环境细菌定殖。通过代谢谱分析，我们表明内生生态位富含有机酸和三羧酸循环的中间产物。能够利用这些酸的环境细菌，如土壤细菌恶臭假单胞菌，很容易定殖于共生体缺失的植物。然而，成功定殖取决于垂直传播的共生体不存在或其VI型分泌系统受损。对于垂直传播的共生关系而言出乎意料的是，这些发现表明微生物间的相互作用，包括拮抗作用，可能在维持共生关系的特异性方面发挥关键作用。然而，合成共生体的低传播率提供了证据，表明传播障碍或瓶颈可能仍然存在，进一步强化了伙伴忠诚度。总之，这些结果突出了互利共生关系背后机制的复杂性，并为细菌叶共生的进化提供了见解。
