Department of Biology, Lund University, Lund, Sweden.
Department of Chemistry and Chemical Biology, McMaster University, Hamilton, Ontario, Canada.
Geobiology. 2022 Sep;20(5):650-666. doi: 10.1111/gbi.12504. Epub 2022 Jun 10.
Mineral-associated organic matter is an integral part of soil carbon pool. Biological processes contribute to the formation of such organo-mineral complexes when soil microbes, and in particular soil fungi, deposit a suite of extracellular metabolic compounds and their necromass on the mineral surfaces. While studied in bulk, micro- to nanoscale fungal-mineral interactions remain elusive. Of particular interest are the mutual effects at the interface between the fungal exometabolites and proximal mineral particles. In this work, we have grown saprotrophic and symbiotic fungi in contact with two soil minerals with contrasting properties: quartz and goethite, on top of X-ray transparent silicon nitride membrane windows and analyzed fungal hyphae by synchrotron-based scanning transmission X-ray microscopy in combination with near edge X-ray fine structure spectroscopy at C(K) and Fe(L) absorption edges. In the resultant chemical maps, we were able to visualize and differentiate organic compounds constituting the fungal cells, their extracellular metabolites, and the exometabolites adsorbing on the minerals. We found that the composition of the exometabolites differed between the fungal functional guilds, particularly, in their sugar to protein ratio and potassium concentration. In samples with quartz and goethite, we observed adsorption of the exometabolic compounds on the mineral surfaces with variations in their chemical composition around the particles. Although we did not observe clear alteration in the exometabolite chemistry upon mineral encounters, we show that fungal-mineral interaction result in reduction of Fe(III) in goethite. This process has been demonstrated for bulk systems, but, to our knowledge, this is the first observation on a single hypha scale offering insight into its underlying biological mechanisms. This demonstrates the link between processes initiated at the single-cell level to macroscale phenomena. Thus, spatially resolved chemical characterization of the microbial-mineral interfaces is crucial for an increased understanding of overall carbon cycling in soil.
矿物相关有机质是土壤碳库的一个组成部分。当土壤微生物（尤其是土壤真菌）在矿物表面沉积一系列细胞外代谢物和它们的坏死物质时，生物过程有助于形成这种有机-矿物复合物。虽然在整体上进行了研究，但微到纳米尺度的真菌-矿物相互作用仍然难以捉摸。特别有趣的是真菌外代谢物和近矿颗粒之间界面的相互作用。在这项工作中，我们在 X 射线透明氮化硅膜窗上生长了腐生菌和共生菌，接触了两种具有不同性质的土壤矿物：石英和针铁矿，并结合同步辐射扫描透射 X 射线显微镜和 C(K)和 Fe(L)吸收边缘的近边 X 射线精细结构光谱分析了真菌菌丝。在得到的化学图谱中，我们能够可视化和区分构成真菌细胞的有机化合物、它们的细胞外代谢物以及吸附在矿物上的外代谢物。我们发现外代谢物的组成在真菌功能群之间存在差异，特别是在糖与蛋白质的比例和钾浓度方面。在含有石英和针铁矿的样品中，我们观察到外代谢物在矿物表面的吸附，其化学组成在颗粒周围发生变化。尽管我们没有观察到矿物接触时外代谢物化学性质的明显变化，但我们表明真菌-矿物相互作用导致针铁矿中的 Fe(III)还原。这个过程已经在体相系统中得到证明，但据我们所知，这是首次在单个菌丝尺度上观察到这一现象，为其潜在的生物学机制提供了深入的了解。这表明了从单细胞水平开始的过程与宏观现象之间的联系。因此，对微生物-矿物界面的空间分辨化学特征的研究对于提高对土壤中整体碳循环的理解至关重要。
