Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling

Abstract

Arbuscular mycorrhizal (AM) fungi are obligate biotrophs that acquire carbon (C) solely from host plants. AM fungi can proliferate hyphae in, and acquire nitrogen (N) from, organic matter. Although they can transfer some of that N to plants, we tested the hypothesis that organic matter is an important N source for the AM fungi themselves. We grew pairs of plants with and without the AM fungus Glomus hoi in microcosms that allowed only the fungus access to a 15 N/ 13 C-labeled organic patch; in some cases, one plant was shaded to reduce C supply to the fungus. The fungal hyphae proliferated vigorously in the patch, irrespective of shading, and increased plant growth and N content; ∼3% of plant N came from the patch. The extraradical mycelium of the fungus was N-rich (3-5% N) and up to 31% of fungal N came from the patch, confirming the hypothesis. The fungus acquired N as decomposition products, because hyphae were not 13 C-enriched. In a second experiment, hyphae of both G. hoi and Glomus mosseae that exploited an organic material patch were also better able to colonize a new host plant, demonstrating a fungal growth response. These findings show that AM fungi can obtain substantial amounts of N from decomposing organic materials and can enhance their fitness as a result. The large biomass and high N demand of AM fungi means that they represent a global N pool equivalent in magnitude to fine roots and play a substantial and hitherto overlooked role in the nitrogen cycle. nutrient capture | organic patches | stable isotopes | fitness A rbuscular mycorrhizal (AM) symbioses, formed by fungi in the Glomeromycota with the majority of land plants (1), are central to the phosphorus cycle: AM fungi (AMF) capture poorly mobile phosphate ions that would be otherwise unavailable to plants via an extensive hyphal network outside the nutrient depletion zone around the root (2). However, they are held to play only a minor role in the N cycle, because they are obligate biotrophs lacking the saprotrophic capability needed to acquire N from organic sources and because both ammonium and especially nitrate ions are relatively mobile in soil, reducing the potential benefit to the plant of fungal-mediated uptake (3). Here we show that AMF proliferate preferentially in a patch of organic material and can acquire a third of their N from that source. We also show that, because AMF hyphae are N-rich in comparison with plants, they are likely to play a large but hitherto unconsidered role in the global N cycle.Nitrogen is a limiting nutrient in many terrestrial ecosystems (4). AMF can transfer inorganic N (NO 3 − or NH 4 + ) to their host plant (5), but because these ions can readily move to the root via diffusion, it has been assumed that roots would not require mycorrhizal assistance to capture inorganic N, particularly because plants that form the AM symbiosis frequently occur in ecosystems with high nitrification rates (6). However, N limitation can occur even in these ecosystems (7) and nitrate acquisition via AMF might offer an adv...

Arbuscular mycorrhizal fungi altered the hypericin, pseudohypericin, and hyperforin content in flowers of Hypericum perforatum grown under contrasting P availability in a highly organic substrate

“…Such effects could depend on both the competition for N and photosynthates between AM fungi and flowers (Johnson et al 1982) and the ability of AM fungi to reduce nutrient deficiency or other stresses for the host plant. The number of flower-bearing stems is determined earlier than the number of flowers per stem (Slafer et al 1996), and AM fungi retain most of the N taken up in organic form for their own growth (Hodge and Fitter 2010). The growth substrate used in the present study was rich in organic matter.…”

Disproportionate single-species contribution to canopy-soil nutrient flux in an Amazonian rainforest

“…Experiments with pairs of plants with and without arbuscular mycorrhiza fungi showed that the fungus increased plant grows and N content (Hodge and Fitter, 2010). A study of babassu palm roots revealed root diameters in excess of 2 mm, which indicates abundance of mycorrhiza, and another study found a characteristic arbuscalar mycorrhizal species composition under babassu dominated sites (unpublished data, Christoph Gehring).…”

Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil

“…Several studies also show that AMF influence bacterial communities inhabiting the rhizosphere and mycorrhizosphere (Ames et al, 1984;Scheublin et al, 2010), including shifts in denitrifying communities (Amora-Lazcano et al, 1998;Veresoglou et al, 2012b). AMF influence the N cycle and can take up significant amounts of nitrogen (Hodge and Fitter, 2010;Veresoglou et al, 2012a). By reducing the availability of soluble N in the soil, AMF could also reduce denitrification and N 2 O emission rates.…”