Joint International Research Laboratory of Global Change and Water Cycle, State Key Laboratory of Hydrology-Water Resources and Hydraulic Engineering, College of Hydrology and Water Resources, Hohai University, Nanjing, China.
State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, Nanjing, China.
Appl Environ Microbiol. 2023 Jul 26;89(7):e0071723. doi: 10.1128/aem.00717-23. Epub 2023 Jul 5.
Submerged macrophytes and their epiphytic microbes form a "holobiont" that plays crucial roles in regulating the biogeochemical cycles of aquatic ecosystems but is sensitive to environmental disturbances such as ammonium loadings. Increasingly more studies suggest that plants may actively seek help from surrounding microbial communities whereby conferring benefits in responding to particular abiotic stresses. However, empirical evidence is scarce regarding how aquatic plants reconstruct their microbiomes as a "cry-for-help" against acute ammonium stress. Here, we investigated the temporal dynamics of the phyllosphere and rhizosphere bacterial communities of following ammonium stress and recovery periods. The bacterial community diversity of different plant niches exhibited opposite patterns with ammonium stress, that is, decreasing in the phyllosphere while increasing in the rhizosphere. Furthermore, both phyllosphere and rhizosphere bacterial communities underwent large compositional changes at the end of ammonium stress, significantly enriching of several nitrifiers and denitrifiers. Meanwhile, bacterial legacies wrought by ammonium stress were detected for weeks; some plant growth-promoting and stress-relieving bacteria remained enriched even after stress disappeared. Structural equation model analysis showed that the reshaped bacterial communities in plant niches collectively had a positive effect on maintaining plant biomass. Additionally, we applied an age-prediction model to predict the bacterial community's successional trajectory, and the results revealed a persistent change in bacterial community development under ammonium treatment. Our findings highlight the importance of plant-microbe interactions in mitigating plant stress and fostering a better understanding of the assembly of plant-beneficial microbes under ammonium stress in aquatic ecosystems. Increasing anthropogenic input of ammonium is accelerating the decline of submerged macrophytes in aquatic ecosystems. Finding efficient ways to release submerged macrophytes from ammonium stress is crucial to maintain their ecological benefits. Microbial symbioses can alleviate abiotic stress in plants, but harnessing these beneficial interactions requires a detailed understanding of plant microbiome responses to ammonium stress, especially over a continuous time course. Here, we tracked the temporal changes in bacterial communities associated with the phyllosphere and rhizosphere of during ammonium stress and recovery periods. Our results showed that severe ammonium stress triggers a plant-driven timely reshaping of the associated bacterial community in a niche-specific strategy. The reassembled bacterial communities could potentially benefit the plant by positively contributing to nitrogen transformation and plant growth promotion. These findings provide empirical evidence regarding the adaptive strategy of aquatic plants whereby they recruit beneficial microbes against ammonium stress.
淹没植物及其附生微生物形成一个“整体共生体”,在调节水生生态系统的生物地球化学循环中起着关键作用,但对铵负荷等环境干扰很敏感。越来越多的研究表明,植物可能会主动寻求周围微生物群落的帮助,从而在应对特定非生物胁迫方面获得益处。然而,关于水生植物如何在急性铵胁迫下作为“呼救”来重建其微生物组的实证证据仍然很少。在这里,我们研究了 在铵胁迫和恢复期间,叶际和根际细菌群落的时间动态。不同植物生境的细菌群落多样性随着铵胁迫表现出相反的模式,即叶际减少而根际增加。此外,在铵胁迫结束时,叶际和根际细菌群落都经历了很大的组成变化,显著富集了一些硝化和反硝化细菌。同时,铵胁迫造成的细菌“遗产”在数周内都被检测到;一些促进植物生长和缓解压力的细菌即使在压力消失后仍然富集。结构方程模型分析表明,植物生境中重塑的细菌群落对维持植物生物量有积极影响。此外,我们应用了一个年龄预测模型来预测细菌群落的演替轨迹,结果表明在铵处理下细菌群落的发展持续发生变化。我们的研究结果强调了植物-微生物相互作用在缓解植物压力方面的重要性,并更好地理解了水生生态系统中铵胁迫下植物有益微生物的组装。人为输入的铵增加正在加速水生生态系统中淹没植物的减少。寻找有效的方法使淹没植物摆脱铵胁迫对于维持它们的生态效益至关重要。微生物共生可以缓解植物的非生物胁迫,但利用这些有益的相互作用需要详细了解植物微生物组对铵胁迫的反应,特别是在连续的时间过程中。在这里,我们跟踪了 在铵胁迫和恢复期间与叶际和根际相关的细菌群落的时间变化。我们的结果表明,严重的铵胁迫会触发一种植物驱动的、特定生境的、及时的相关细菌群落重塑策略。重新组装的细菌群落可能通过对氮转化和植物生长促进的积极贡献,对植物有益。这些发现为水生植物应对铵胁迫时招募有益微生物的适应性策略提供了经验证据。