Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi

Atmospheric nitrogen (N) deposition has increased dramatically since preindustrial times and continues to increase across many regions of the Earth. In temperate forests, this agent of global change has increased soil carbon (C) storage, but the mechanisms underlying this response are not understood. One long-standing hypothesis proposed to explain the accumulation of soil C proposes that higher inorganic N availability may suppress both the activity and abundance of fungi which decay lignin and other polyphenols in soil. In field studies, elevated rates of N deposition have reduced the activity of enzymes mediating lignin decay, but a decline in the abundance of lignolytic fungi has not been definitively documented to date. Here, we tested the hypothesis that elevated rates of anthropogenic N deposition reduce the abundance of lignolytic fungi. We conducted a field experiment in which we compared fungal communities colonizing low-lignin, high-lignin, and wood substrates in a northern hardwood forest that is part of a long-term N deposition experiment. We reasoned that, if lignolytic fungi decline under experimental N deposition, this effect should be most evident among fungi colonizing high-lignin and wood substrates. Using molecular approaches, we provide evidence that anthropogenic N deposition reduces the relative abundance of lignolytic fungi on both wood and a high-lignin substrate. Furthermore, experimental N deposition increased total fungal abundance on a low-lignin substrate, reduced fungal abundance on wood, and had no significant effect on fungal abundance on a high-lignin substrate. We simultaneously examined these responses in the surrounding soil and forest floor, in which we did not observe significant reductions in the relative abundance of lignolytic fungi or in the size of the fungal community; however, we did detect a change in community composition in the forest floor that appears to be driven by a shift away from lignolytic fungi and towards cellulolytic fungi. Our results provide direct evidence that reductions in the abundance of lignolytic fungi are part of the mechanism by which anthropogenic N deposition increases soil C storage.

自工业革命前以来，大气氮（N）沉降已大幅增加，且在全球诸多区域仍持续攀升。在温带森林中，这一全球变化驱动因子提升了土壤碳（C）储量，但其背后的作用机制尚未明晰。有一项长期存在的假说试图解释土壤碳储量的累积过程，该假说提出，更高的无机氮有效性可能会抑制降解土壤中木质素与其他多酚类物质的真菌的活性与种群丰度。野外研究表明，高氮沉降速率会降低介导木质素降解的酶的活性，但截至目前，尚未有确凿证据证实木质素降解真菌（lignolytic fungi）的丰度出现下降。本研究旨在验证“人为高氮沉降会降低木质素降解真菌的丰度”这一假说。我们依托一项长期氮沉降试验平台中的北方硬叶林开展野外实验，对比了定殖于低木质素基质、高木质素基质以及木质基质的真菌群落。我们推测，若实验性氮沉降会导致木质素降解真菌丰度下降，那么该效应在定殖于高木质素基质与木质基质的真菌群落中应最为显著。通过分子生物学方法，我们证实人为氮沉降会降低木质素降解真菌在木质基质与高木质素基质上的相对丰度。此外，实验性氮沉降提升了低木质素基质上的总真菌丰度，降低了木质基质上的真菌丰度，而对高木质素基质上的真菌丰度无显著影响。我们同时对周边土壤与森林枯落层进行了检测，未发现木质素降解真菌的相对丰度或真菌群落规模出现显著下降，但我们确实在森林枯落层中检测到了群落组成的变化，这一变化似乎是由真菌群落从木质素降解真菌向纤维素降解真菌（cellulolytic fungi）转变所驱动的。本研究结果提供了直接证据，证明木质素降解真菌丰度的下降正是人为氮沉降提升土壤碳储量的作用机制之一。