Department of Environmental Microbiology, Helmholtz Centre for Environmental Researchgrid.7492.8-UFZ, Leipzig, Germany.
Department of Solar Materials, Helmholtz Centre for Environmental Researchgrid.7492.8-UFZ, Leipzig, Germany.
mBio. 2022 Jun 28;13(3):e0076922. doi: 10.1128/mbio.00769-22. Epub 2022 May 31.
Anoxic microsites arising in fungal biofilms may foster the presence of obligate anaerobes. Here, we analyzed whether and to which degree hyphae of Coprinopsis cinerea thriving in oxic habitats enable the germination, growth, and dispersal of the obligate anaerobic soil bacterium Clostridium acetobutylicum. Time-resolved optical oxygen mapping, microscopy, and metabolite analysis revealed the formation and persistence of anoxic circum hyphal niches, allowing for spore germination, growth, and fermentative activity of the obligate anaerobe in an otherwise inhabitable environment. Hypoxic liquid films containing 80% ± 10% of atmospheric oxygen saturation around single air-exposed hyphae thereby allowed for efficient clostridial dispersal amid spatially separated (>0.5 cm) anoxic sites. Hyphae hence may serve as good networks for the activity and spatial organization of obligate anaerobic bacteria in oxygenated heterogeneous environments such as soil. Although a few studies have reported on the presence of anoxic microniches in fungal biofilms, knowledge of the effects of fungal oxygen consumption on bacterial-fungal interactions is limited. Here, we demonstrate the existence and persistence of oxygen-free zones in air-exposed mycelia enabling spore germination, growth, fermentative activity, and dispersal of the obligate anaerobe. Our study points out a previously overlooked role of aerobic fungi in creating and bridging anoxic microniches in ambient oxic habitats. Air-exposed hyphae hence may act as a scaffold for activity and dispersal of strictly anaerobic microbes. Given the short-term tolerance of strict anaerobes to oxygen and reduced oxygen content in the mycosphere, hyphae can promote spatial organization of both obligate anaerobic and aerobic bacteria. Such finding may be important for a better understanding of previously observed co-occurrences of aerobes and anaerobes in well-aerated habitats such as upland soils.
真菌生物膜中出现的缺氧微区可能会促进专性厌氧菌的存在。在这里，我们分析了在好氧生境中生长的毛头鬼伞菌丝是否以及在何种程度上能够使专性厌氧菌丁酸梭菌发芽、生长和扩散。时间分辨的光学氧映射、显微镜和代谢物分析揭示了缺氧环菌丝生境的形成和持续存在，从而允许孢子发芽、生长和专性厌氧菌在原本无法居住的环境中进行发酵活动。含有 80%±10%大气氧饱和度的缺氧液体薄膜围绕单个暴露于空气的菌丝形成，从而允许在空间上分离（>0.5 厘米）的缺氧部位之间高效地进行梭状芽孢杆菌分散。菌丝因此可以作为好的网络，用于在有氧异质环境（如土壤）中活动和空间组织专性厌氧菌。虽然有一些研究报告了真菌生物膜中缺氧微生境的存在，但对真菌耗氧对细菌-真菌相互作用的影响知之甚少。在这里，我们证明了在暴露于空气的菌丝中存在并持续存在无氧区，从而使孢子发芽、生长、发酵活性和专性厌氧菌的扩散成为可能。我们的研究指出了以前被忽视的好氧真菌在创造和桥接环境有氧栖息地中的缺氧微生境中的作用。暴露于空气的菌丝因此可以作为严格厌氧菌活动和扩散的支架。鉴于严格厌氧菌对氧气的短期耐受性和菌根中氧气含量降低，菌丝可以促进专性厌氧菌和需氧菌的空间组织。这一发现对于更好地理解在好氧栖息地（如旱地土壤）中观察到的好氧菌和厌氧菌的共存现象可能很重要。
