Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California, USA.
Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA.
Appl Environ Microbiol. 2022 Mar 22;88(6):e0232021. doi: 10.1128/aem.02320-21. Epub 2022 Feb 9.
Phenazines are a class of bacterially produced redox-active natural antibiotics that have demonstrated potential as a sustainable alternative to traditional pesticides for the biocontrol of fungal crop diseases. However, the prevalence of bacterial resistance to agriculturally relevant phenazines is poorly understood, limiting both the understanding of how these molecules might shape rhizosphere bacterial communities and the ability to perform a risk assessment for off-target effects. Here, we describe profiles of susceptibility to the antifungal agent phenazine-1-carboxylic acid (PCA) across more than 100 bacterial strains isolated from a wheat field where PCA producers are indigenous and abundant. We found that Gram-positive bacteria are typically more sensitive to PCA than Gram-negative bacteria, and there was significant variability in susceptibility both within and across phyla. Phenazine-resistant strains were more likely to be isolated from the wheat rhizosphere, where PCA producers were also more abundant, compared to bulk soil. Furthermore, PCA toxicity was pH-dependent for most susceptible strains and broadly correlated with PCA reduction rates, suggesting that uptake and redox-cycling were important determinants of phenazine toxicity. Our results shed light on which classes of bacteria are most likely to be susceptible to phenazine toxicity in acidic or neutral soils. In addition, the taxonomic and phenotypic diversity of our strain collection represents a valuable resource for future studies on the role of natural antibiotics in shaping wheat rhizosphere communities. Microbial communities contribute to crop health in important ways. For example, phenazine metabolites are a class of redox-active molecules made by diverse soil bacteria that underpin the biocontrol of diseases of wheat and other crops. Their physiological functions are nuanced. In some contexts, they are toxic. In others, they are beneficial. While much is known about phenazine production and the effect of phenazines on producing strains, our ability to predict how phenazines might shape the composition of environmental microbial communities is poorly constrained. In addition, phenazine prevalence in the rhizosphere has been predicted to increase in arid soils as the climate changes, providing an impetus for further study. As a step toward gaining a predictive understanding of phenazine-linked microbial ecology, we document the effects of phenazines on diverse bacteria that were coisolated from a wheat rhizosphere and identify conditions and phenotypes that correlate with how a strain will respond to phenazines.
吩嗪类是一类由细菌产生的氧化还原活性天然抗生素，它们具有替代传统农药防治真菌作物病害的潜力，是一种可持续的选择。然而，对于农业上相关的吩嗪类抗生素，细菌的抗药性的普遍性还了解甚少，这既限制了我们对这些分子如何影响根际细菌群落的理解，也限制了对非靶标效应进行风险评估的能力。在这里，我们描述了来自一个小麦田的 100 多个细菌菌株对农用吩嗪-1-羧酸（PCA）的敏感性谱，该田块中 PCA 的产生菌是土著且丰富的。我们发现，革兰氏阳性菌通常比革兰氏阴性菌对 PCA 更敏感，而且在同一门内和跨门之间都存在显著的敏感性变异性。与土壤相比，在富含 PCA 产生菌的小麦根际中更容易分离到抗 PCA 的菌株。此外，对于大多数敏感菌株，PCA 的毒性随 pH 值而变化，并且与 PCA 的还原速率广泛相关，这表明摄取和氧化还原循环是吩嗪毒性的重要决定因素。我们的结果阐明了在酸性或中性土壤中哪些类群的细菌最容易受到吩嗪毒性的影响。此外，我们的菌株收集的分类学和表型多样性代表了未来研究天然抗生素在塑造小麦根际群落中的作用的宝贵资源。 微生物群落以重要的方式促进作物健康。例如，吩嗪代谢物是由多种土壤细菌产生的一类氧化还原活性分子，它们是小麦和其他作物生物防治疾病的基础。它们的生理功能很微妙。在某些情况下，它们是有毒的。在其他情况下，它们是有益的。虽然人们对吩嗪的产生及其对产生菌株的影响有了很多了解，但我们预测吩嗪如何塑造环境微生物群落组成的能力受到很大限制。此外，随着气候变化，干旱土壤中根际吩嗪的流行度预计会增加，这为进一步研究提供了动力。作为对与吩嗪相关的微生物生态学进行预测性理解的一个步骤，我们记录了从小麦根际共同分离出的不同细菌对吩嗪的影响，并确定了与菌株对吩嗪的反应相关的条件和表型。
