Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019 Jun 21:2:233.
doi: 10.1038/s42003-019-0481-8. eCollection 2019.

Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition

Rachel Hestrin  1 , Edith C Hammer  2 , Carsten W Mueller  3 , Johannes Lehmann  1   4   5
Affiliations

Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition

Rachel Hestrin et al. Commun Biol. .

Abstract

Nitrogen availability often restricts primary productivity in terrestrial ecosystems. Arbuscular mycorrhizal fungi are ubiquitous symbionts of terrestrial plants and can improve plant nitrogen acquisition, but have a limited ability to access organic nitrogen. Although other soil biota mineralize organic nitrogen into bioavailable forms, they may simultaneously compete for nitrogen, with unknown consequences for plant nutrition. Here, we show that synergies between the mycorrhizal fungus Rhizophagus irregularis and soil microbial communities have a highly non-additive effect on nitrogen acquisition by the model grass Brachypodium distachyon. These multipartite microbial synergies result in a doubling of the nitrogen that mycorrhizal plants acquire from organic matter and a tenfold increase in nitrogen acquisition compared to non-mycorrhizal plants grown in the absence of soil microbial communities. This previously unquantified multipartite relationship may contribute to more than 70 Tg of annually assimilated plant nitrogen, thereby playing a critical role in global nutrient cycling and ecosystem function.

Keywords: Arbuscular mycorrhiza; Element cycles; Soil microbiology.

PubMed Disclaimer

Conflict of interest statement

Competing interestsThe authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Multipartite synergies between AM fungi and soil microbial communities increase plant biomass and N acquisition from organic matter. a Mesocosm design. b Plants acquired more N from organic matter in the presence of AM fungi and soil microbial communities. c Plants grown with both AM fungi and soil microbes acquired more N than expected based on the sum of N acquired by control plants and those grown with AM fungi or soil microbes alone. d AM colonization is associated with greater plant biomass. e AM plants grown with soil microbes derived a greater proportion of their total N from organic matter than control plants and plants grown with AM fungi or soil microbial communities alone. Significance levels are indicated with the following symbols: ·p < 0.1, *p < 0.05, **p < 0.01, ***p < 0.001 and denote the results of a Tukey’s HSD test performed on log-transformed data (b, d), an unpaired t test (c), and a Tukey’s HSD test performed on untransformed data (e). Error bars represent the standard error (n = 7 biologically independent samples)
Fig. 2
Fig. 2
Relative 15N enrichment of fungal hyphae, plant roots, and plant aboveground tissue. Lowercase letters denote the results of a Tukey’s HSD test comparing log-transformed mean δ 15N values of fungal hyphae; uppercase letters denote the results of a Tukey’s HSD test comparing mean δ 15N values of plant tissues (p < 0.05). Error bars represent the standard error (n = 7 biologically independent samples)
Fig. 3
Fig. 3
Microbial lipid biomass present in organic matter. Phospholipid fatty acid (PLFA) analysis was used to measure microbial lipid biomass in the organic matter harvested from mesocosms containing AM plants only and both AM plants and free-living soil microbes from grasslands fertilized with 0, 28, and 196 kg N ha−1 per year. Significant differences between total microbial lipid biomass measured through a Tukey’s HSD test performed on log-transformed PLFA sums from each treatment are indicated by the following symbols: ·p < 0.1, *p < 0.05, **p < 0.01. Error bars represent the standard error of the mean of total microbial PLFAs measured in each mesocosm type (n = 7 biologically independent samples). Microbial lipid biomass associated with AM fungi, bacteria, and non-AM fungi is indicated in yellow, blue, and orange bars, respectively. Lowercase letters above the upper right-hand corner of each bar denote the results of Tukey’s HSD tests performed only for PLFAs of the same subtype (AM fungi, bacteria, or non-AM fungi; p < 0.05). N enrichment did not result in a substantial difference in the ratio of fungal:bacterial lipids present in mesocosms containing AM plants and microbial inoculum from grassland fields. However, the ratios of AM fungal:bacterial lipids in these mesocosms were higher than in mesocosms inoculated only with AM fungi, suggesting that the presence of soil microbial communities benefitted the AM fungi in addition to benefitting the plant. It is not clear whether this was a direct benefit to the AM fungi, or whether it was modulated through increased provision of plant photosynthates
Fig. 4
Fig. 4
Mean relative 13C enrichment of microbial biomass lipids measured through phospholipid fatty acid (PLFA) analysis. Since organic matter was enriched with 13C and plant photosynthates were depleted in 13C, lower PLFA δ 13C values suggest that microbes derived a greater proportion of their C from plant photosynthates. Letters denote the results of a Tukey’s HSD test performed on log-transformed data; error bars represent the standard error (p < 0.01, n = 7 biologically independent samples)
Fig. 5
Fig. 5
Light microscopy, scanning electron microscopy (SEM), and nano-scale secondary ion mass spectrometry (NanoSIMS) images of enriched organic matter, AM fungi, and soil microbes. a Light microscopy image of fungi and soil microbes grown in 15N13C enriched organic matter. The white square demarcates the 30 × 30 µm region from which the NanoSIMS images were collected. b SEM image of the same sample. The black square demarcates the same 30 × 30 µm region from which the NanoSIMS images were collected. The dense cluster towards the top of the image is organic matter. The 5-10 µm thick strands extending below are fungal hyphae. c SEM image of the exact region from which NanoSIMS images were collected. A cluster of bacterial cells is located in the top left corner. The 5–10 µm thick strands extending across the image are fungal hyphae. 15N13C enriched organic matter is located in the upper left quadrant of the image. d NanoSIMS images of 12C15N/12C14N and (e) 13C/12C isotope ratios of fungi, bacteria, and organic matter are shown in a color scale with natural abundance values in blue (.003676 and .0111802, respectively) and high enrichment in purple. Bacterial 15N incorporation was highly heterogeneous between cells, even within the distance of a few microns. Fungal 15N incorporation was relatively even across hyphae. Scale bars, 30 µm (a, b) and 10 µm (c–e)
Fig. 6
Fig. 6
Nonmetric multidimensional scaling (NMDS) plot of microbial community composition based on PLFA profiles. Microbial community composition in mesocosms containing AM plants only (yellow symbol) and those containing AM plants and soil microbes that developed under an environmental N gradient of 0, 28, and 196 kg N ha−1 per year (light, medium, and dark green symbols, respectively) varied significantly (p < 0.01). Error bars show the standard error of the mean NMDS scores (n = 7 biologically independent samples)
Fig. 7
Fig. 7
Microbial net N mineralization potential. In the absence of plants and AM fungi, net N mineralization rates did not vary between microbial inocula sampled from switchgrass fields fertilized with 0, 28, and 196 kg N ha−1 per year. Lower N mineralized in treatments containing microbial inocula compared to controls suggests that some of the N mineralized was immobilized by microbes. Statistical significance is based on a Tukey’s HSD test (p < 0.001); error bars represent the standard error (n = 4 biologically independent samples)
See this image and copyright information in PMC

References

    1. Vitousek P, Howarth R. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemisty. 1991;13:87–115. doi: 10.1007/BF00002772. - DOI
    1. LeBauer DS, Treseder KK. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology. 2008;89:371–379. doi: 10.1890/06-2057.1. - DOI - PubMed
    1. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis 3rd edn, (Academic Press, London 2008).
    1. Govindarajulu, M. etal. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature435, 819–823 (2005). - PubMed
    1. Mader P, et al. Transport of N-15 from a soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol. 2000;146:155–161. doi: 10.1046/j.1469-8137.2000.00615.x. - DOI

Publication types