Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.
Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA; Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA, USA.
Curr Biol. 2022 Jan 24;32(2):275-288.e5. doi: 10.1016/j.cub.2021.11.002. Epub 2021 Nov 22.
Many environmentally and clinically important fungi are sensitive to toxic, bacterially produced, redox-active molecules called phenazines. Despite being vulnerable to phenazine assault, fungi inhabit microbial communities that contain phenazine producers. Because many fungi cannot withstand phenazine challenge but some bacterial species can, we hypothesized that bacterial partners may protect fungi in phenazine-replete environments. From a single soil sample, we were able to co-isolate several such physically associated pairings. We discovered the novel species Paraburkholderia edwinii and demonstrated it can protect a co-isolated Aspergillus species from phenazine-1-carboxylic acid (PCA) by sequestering it, acting as a toxin sponge; in turn, it also gains protection. When challenged with PCA, P. edwinii changes its morphology, forming aggregates within the growing fungal colony. Further, the fungal partner triggers P. edwinii to sequester PCA and maintains conditions that limit PCA toxicity by promoting an anoxic and highly reducing environment. A mutagenic screen of P. edwinii revealed this protective program depends on the stress-inducible transcriptional repressor HrcA. We show that one relevant stressor in response to PCA challenge is fungal acidification and that acid stress causes P. edwinii to behave as though the fungus were present. Finally, we reveal this phenomenon as widespread among Paraburkholderia with moderate specificity among bacterial and fungal partners, including plant and human pathogens. Our discovery suggests a common mechanism by which fungi can gain access to phenazine-replete environments and provides a tractable model system for its study. These results have implications for how microbial communities in the rhizosphere as well as in plant and human infection sites negotiate community membership via a chemical dialectic.
许多对环境和临床都很重要的真菌对毒性的、细菌产生的、氧化还原活性分子（称为吩嗪）敏感。尽管真菌易受吩嗪的攻击，但它们栖息在含有吩嗪产生菌的微生物群落中。因为许多真菌无法承受吩嗪的挑战，但有些细菌可以，所以我们假设细菌伙伴可能会在富含吩嗪的环境中保护真菌。从一个单一的土壤样本中，我们能够共分离出几种这样的物理相关配对。我们发现了一种新的物种 Paraburkholderia edwinii，并证明它可以通过螯合、充当毒素海绵来保护与其共分离的曲霉属物种免受吩嗪-1-羧酸（PCA）的侵害；反过来，它也获得了保护。当受到 PCA 的挑战时，P. edwinii 会改变其形态，在真菌菌落中形成聚集体。此外，真菌伙伴触发 P. edwinii 螯合 PCA，并通过促进缺氧和高度还原的环境来维持限制 PCA 毒性的条件。对 P. edwinii 的诱变筛选显示，这种保护程序依赖于应激诱导的转录阻遏物 HrcA。我们表明，一种与 PCA 挑战相关的相关应激源是真菌酸化，而酸应激会导致 P. edwinii 表现得好像真菌存在一样。最后，我们揭示了这种现象在 Paraburkholderia 中很普遍，并且在细菌和真菌伙伴之间具有中等特异性，包括植物和人类病原体。我们的发现表明，真菌可以进入富含吩嗪的环境的一种常见机制，并为其研究提供了一个可行的模型系统。这些结果对根际微生物群落以及植物和人类感染部位如何通过化学对话来协商社区成员资格具有重要意义。
