The nitrogen dilemma: food or the environment, Stewart & Lal 2017
Nitrogen (N) is the most important essential element for crop production because it is required in large amounts and is nearly always the first nutrient that becomes limiting after an ecosystem is converted to cropland. Cereal grains provide about 50% of the world’s calories, and their production has become largely dependent on the use of synthetic N fertilizer. However, fertilizer N not used by plants can degrade the environment and negatively impact both people and ecosystems. In addition, efficient use of N fertilizer generally requires phosphorus (P) fertilizer which is made from rock phosphate derived from mines. Therefore, huge amounts of N and P from outside sources are being added to the environment each successive year leading to additional environmental concerns [Stewart & Lal 2017: 124A].
This article articulates a presumed “nitrogen dilemma,” as described above, that, on the one hand, agriculture requires increasing amounts of nitrogen and phosphorus fertilizer, especially as the population surges toward 10 billion. On the other hand, ongoing fertilizer application will lead to increasingly polluted and impaired fresh waters around the world, increased greenhouse gas emissions, and over-reliance on limited supplies of mined phosphorus.
The difficulty of reducing nitrogen inputs is twofold according to the article: First, farmers cannot know exactly how much nitrogen their crops will need because yield depends on water supply and respiration rates, and only indirectly on nitrogen availability. Therefore, farmers are reluctant to limit fertilizer input for fear it could in turn limit water utilization. “Because N is usually the first limiting factor other than water, most farmers want to make sure they have enough N available to fully utilize the water” [p.126A]. Second, nutrient-polluted waters is a local problem, and therefore most likely requires a local political solution, rather than being manageable through national regulations. Local policy solutions will happen only when enough people feel the direct effects of the problem locally and demand action.
Curiously, the article fails to mention the farming practices that reduce the need for fertilizers, maximize the soil’s water-holding capacity, and cool the soil through continuous vegetative cover. Practices designed to enhance soil organic matter, such as cover-cropping and replacing synthetic fertilizer input with compost, manure and crop residues, can achieve the same goals that nitrogen fertilizer is supposed to address.
…it is water that determines yield, and the amount of water available for a crop is beyond control of the farmer, even if the crop is irrigated. This is because it is only the amount of water transpired by the growing crop that determines the amount of biomass produced by photosynthesis, and this is affected not only by the amount of water available but on other climatic factors such as temperature, radiation, humidity, and wind [Steward & Lal 2017: 126A].
We argue that there is no nitrogen dilemma unless we cling to the idea that industrial agriculture is the only way forward despite its increasingly apparent fragility, while rejecting the potential of multifunctional, regenerative agriculture to broadly achieve our production and environmental goals.
Sustainability challenges of phosphorus and food: solutions from closing the human phosphorus cycle, Childers 2011
Our review of estimates of P recycling in the human P cycle show considerable variability and uncertainty, but today it appears that only about one-quarter of the fertilizer P used in agriculture is recycled back to fields. The rest is lost to the cycle, and much of this loss ends up in waterways, causing expensive eutrophication problems. As with other nonrenewable natural resources, a sustainable P supply is not assured, and some projections show economically viable mineral reserves being depleted within decades. In addition to our review of human effects on the global P cycle, we present a number of sustainable solutions that involve closing the loop on the human P cycle. Some of these solutions are relatively straightforward but many involve overcoming considerable infrastructural or institutional inertia [Childers 2011: 123].
Economically viable mineral phosphorus reserves may become depleted within decades, threatening global crop production for a growing world population. The authors discuss this problem in relation to human P cycle, where the vast majority of mined phosphorus is not recycled back onto farm fields, but is released more or less irretrievably into the environment, polluting water bodies. “There are considerable social and environmental costs of P being lost from the currently ‘open’ human P cycle” [Childers 2011: 120].
The authors present several options for closing the human P cycle at the points of agricultural production, distribution and consumption, and human waste treatment. These options include reducing fertilizer application rates to better match plant needs, reducing erosion rates, reducing food waste, and recycling human urine, which is rich in phosphorus and nitrogen. The authors state that their list of solutions is not exhaustive, but rather is meant to stimulate others to think about the sustainability challenges of the human P cycle. Indeed, missing in this paper’s list of solutions is a discussion of the role of fungi, which can access otherwise inaccessible soil phosphorus through symbiosis with plants.
A broken biogeochemical cycle, Elser & Bennett 2011
Consider the fate of the approximately 17.5 million tonnes of phosphorus mined in 2005, analysed in the paper by Cordell et al. About 14 million tonnes of this were used in fertilizer (much of the rest went into cattle-feed supplements, food preservatives, and the production of detergents and industrial cleaning agents) but only about 3 million tonnes made it to the fork (or chopstick). The largest loss — around 8 million tonnes — was directly from farms through soil leaching and erosion” [Elser & Bennett 2011: 30].
To handle the twin problems of phosphorus pollution and scarcity, strategies for phosphorus conservation and recycling are urgently needed.
The solutions to these problems lie in recapturing and recycling phosphorus, moving it from where there is too much to where there is too little, and developing ways to use it more efficiently. Many strategies are simple and readily available, even for poor farmers and developing economies [Elser & Bennett 2011: 30].
The authors’ solutions include: widespread adoption of agricultural conservation practices, reduction of food waste (at least in part by producing food within or closer to cities), recycling human waste, reducing meat consumption, recovering nutrients from confined livestock facilities (such as through bioreactors), and genetically engineering plants and animals to require lower phosphorus inputs. No mention in this article of the role of plant-fungi symbiosis in accessing phosphorus in the soil.
Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning, Leake 2004
Two major groups of mycorrhizal fungi are arbuscular mycorrhiza (AM) and ectomycorrrhiza (EM). Both form a symbiosis with plants by colonizing their roots and creating an interface where carbon from the plant can be exchanged for phosphorus, nitrogen and other nutrients from the soil and transferred to the plant by the fungi. The extraradical mycorrhizal mycelium (ERMM), which are the vast portion of the fungal network that branches out into the soil, is difficult to study and has therefore been considered the “hidden half” of the symbiosis.
Progress in understanding the nature, extent, functioning, and identity of mycorrhizal fungal networks has been seriously hampered by the difficulties inherent in observing and studying mycelial systems without disturbing and destroying them.… As a consequence, the external mycelium, which is the fungal structure of mycorrhiza that is most intimately associated with the soil and furthest from the roots, and by implication the most critical for nutrient uptake, is normally overlooked and has been rarely recorded. Only in the past decade have studies started to focus specifically on the extent and functioning of ERMM in the field [Leake 2004: 1017].
This article highlights the significant yet overlooked role of mycorrhizal fungi in ecosystem functioning and reviews some advances in the techniques used to study these hidden powerhouses.
ERMM is the hidden power behind plant community composition and ecosystem functioning through the major processes it carries out, such as nutrient uptake, weathering of minerals, soil aggregate stability, and the way in which it alters competition between plants [Leake 2004: 1039].
The symbiosis with plants is the source of power for these fungi, given that the carbon received from plant hosts is practically inexhaustible and costs the plants little.
Despite the substantial biomass and associated C drain on their hosts, the actual “cost” of mycorrhiza to plants may be negligible because mycorrhizal colonization can increase the rate of photosynthesis (Wright et al. 1998), alleviate shoot N and P limitation, and cause a substantial increase in leaf area arising from improved nutrition (Read and Perez-Moreno 2003) [Leake 2004: 1021].
The empowerment of mycorrhizal networks with substantial amounts of host-derived C allows them to play central roles in major biogeochemical cycles [Leake 2004: 1030].
The article concludes by emphasizing the importance for sustainable agriculture of a broader public understanding of the role of mycorrhiza for improving soil health and crop yields.
AM [arbuscular mycorrhizal] hyphal lengths in soil show strong positive correlations with soil-aggregate stability (Rillig et al. 2002; Kabir and Koide 2002), P uptake efficiency (Schweiger and Jakobsen 2000), and crop-yield improvements (Kabir and Koide 2002). Interest in the development of less intensive management systems is presenting new opportunities for adapting agricultural production systems to enhance these benefits that can be gained from AM networks. Substantial improvements in “soil health” and AM functioning in field crops are gained by the doubling of lengths of AM hyphae in soil when tillage is reduced (Kabir et al. 1998a, 1998b). Similar gains are achieved by growth of AM-compatible cover crops in place of winter fallow (Kabir and Koide 2002) [Leake 2004: 1038].
ERMM [extraradical mycorrhizal mycelium, or fungi] is the hidden power behind plant community composition and ecosystem functioning through the major processes it carries out, such as nutrient uptake, weathering of minerals, soil aggregate stability, and the way in which it alters competition between plants [Leake 2004: 1039].
Mycorrhizal symbioses influence the trophic structure of the Serengeti, Stevens 2018
Our analysis shows that inputs of phosphorus through arbuscular mycorrhizal symbioses substantially increase the ability of plants to grow and maintain nutritional quality, cascading through the biomass of consumers and predators in the ecosystem. Although they account for less than 1% of the total modelled biomass, the predicted nutritional benefit provided by arbuscular mycorrhizal fungi increased the biomass of macro-organisms in the Serengeti by 48%. When considering the management of biodiversity, future ecosystem models should account for the influence of arbuscular mycorrhizal fungi on all trophic levels [Stevens 2018: 536].
More than 70% of all angiosperm families form AM symbioses (Brundrett, 2009), and these symbioses are often essential for plant nutrition (Marschner & Dell, 1994). Mycorrhizal symbioses also improve plant tolerance to drought (Augé, 2001) and resistance to pathogens (Cameron, Neal, van Wees, & Ton, 2013) [Stevens 2018: 537].
Plant taxa vary in the degree to which they depend upon mycorrhizas; but in general, AM symbioses are essential for the nutrition of tropical plants, and warm season grasses are often highly dependent on mycorrhizas, acquiring up to 90% of their phosphorus requirements from AM fungi [Stevens 2018: 537].
Thirty years ago, McNaughton, Ruess, and Seagle (1988) concluded that large mammals have a major organising effect in the Serengeti ecosystem. From our analysis, we can conclude that AM fungi also play a critical role in the trophic structure of the Serengeti. Our model simulations suggest that although AM fungi account for less than 1% of the total biomass, phosphorus supplied by AM symbioses sustains half the vegetation biomass, and accordingly, half of the biomass of iconic migratory herbivores and one-third of the carnivore biomass [Stevens 2018: 542].
The distribution of soil phosphorus in the Serengeti, transported through AM symbioses and accelerated by migratory ungulates, may be a significant driver of plant diversity and ultimately mammalian carrying capacity (Anderson et al., 2007; McNaughton, Zuniga, McNaughton, & Banyikwa, 1997). Without AM fungal inputs of phosphorus, these nutrient diffusion gradients would undoubtedly decline [Stevens 2018: 543].
Rock-eating fungi, Jongmans 1997
Under a microscope, tiny tunnels can be seen in mineral particles from conifer forest soil. Scientists believe it is mycorrhizal fungi penetrating these particles by excreting organic acids in order to mine nutrients for their plant hosts. An estimated 150 meters of pores are bored by fungi per year per liter of E-horizon (layer that has been leached of mineral and/or organic content, leaving silicate) soil.
Photo credit: Jongmans 1997. “Scanning electron micrograph, showing 4–6-mm-thick hyphae entering a calcium feldspar at a granite surface near Lunsen, Sweden” [Jongman 1997].
The role of community and population ecology in applying mycorrhizal fungi for improved food security, Rodriguez & Sanders 2015
Given that nitrogen and phosphorus are the most limiting nutrients for crop growth, that global phosphorus supplies are becoming exhausted while the human population rapidly expands, and that arbuscular mycorrhizal fungi (AMF) symbioses improve crop phosphorus acquisition, AMF symbioses have a major role to play in current and future crop production.
The potential of AMF to help increase global food security lies in the fact that all globally important food crops naturally form this symbiosis and the fungi help plants more efficiently obtain phosphate from the soil (Smith and Read, 2008). Stocks of phosphate fertilizer are rapidly being depleted (Gross, 2010). There is a simultaneous increase in demand for phosphate to help feed the growing population (Gilbert, 2009). These two combined factors represent a major threat to global food security; a threat that can potentially be reduced by better phosphate acquisition through the AM[F] symbiosis. The potential of AMF to contribute to improved crop yields has been known for decades [Rodriquez & Sanders 2015: 1054].
However, for the widespread adoption of AMF inoculation to be effective and safe, a better understanding is needed of ecological principles related to soil fungi. The authors note that few studies have linked crop yield increases with successful colonization by an introduced AMF, and they outline several challenges and questions that should be resolved to pursue this promising technique more broadly. For example, they ask whether introduced AMF establish well, and how they affect native AMF populations, and how genetic diversity in AMF populations variously affects different crops.
Stocks of phosphate fertilizer are rapidly being depleted (Gross, 2010). There is a simultaneous increase in demand for phosphate to help feed the growing population (Gilbert, 2009). These two combined factors represent a major threat to global food security; a threat that can potentially be reduced by better phosphate acquisition through the [arbuscular mycorrhizal fungi] symbiosis [Rodriquez & Sanders 2015: 1054].
Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils, Rashid 2016
The paper argues for the use of bacterial and fungal inoculants in combination with organic amendments and cover crops to regenerate degraded soils. In order to produce enough food for a growing global population on ubiquitously degraded soils, synthetic fertilizers will be in increasingly high demand. However, these fertilizers require copious amounts of non-renewable energy to manufacture, and become pollutants when used. Here, the authors explain how bacteria and fungi make nutrients available to plants and how facilitate soil aggregation.
Meta-analysis of biofertilizer application in agriculture, Schutz 2018
Given the global decline of reserves of both rock phosphate and fossil fuel, this study poses the question – to what extent can microbial inoculants replace/reduce the use of synthetic fertilizer? The authors find that “dryland agriculture can beneﬁt most from biofertilizers [microbial inoculants used as fertilizers]. Due to climate change, in the future there will be even more dryland areas globally. Biofertilizers are thus a promising option for sustainable agriculture” [Schutz 2018: 11]. More specifically:
Our comprehensive meta-analysis with studies from all over the world revealed that biofertilizers were found to be most eﬀective in dry climates. Biofertilizer also improved PUE [phosphorus use efficiency] and NUE [nitrogen use efficiency] greatly. Furthermore, we found that biofertilizers possessing both N ﬁxing and P solubilizing traits have the highest potential to improve the crop yields. Interestingly, AMFs, known for facilitating P nutrient uptake in plants, were on par with applications of biofertilizers with the combined traits of N ﬁxation and P solubilization, indicating the big potential of AMFs as sole biofertilizer for most crops and climatic situations [Schutz 2018: 5].
Future Directions International Strategic Directions Paper: Agricultural Application of Mycorrhizal Fungi to Increase Crop Yields, Promote Soil Health and Combat Climate Change, Johns 2014
There are a number of agricultural practices that will enhance fungi colonisation. Wherever possible, of course, the full range of critical soil health processes that govern productivity should be allowed to regenerate agricultural ecologies naturally. It may, however, be necessary or more practical to inoculate seed with fungi spores in order to recover degraded soils. A number of farmers in the Great Southern agricultural region of Western Australia are undertaking this course of action. Finding themselves confronted with an unsustainable spiral of ever-increasing commercial fertiliser costs and uneconomic or diminishing crop yields, it was realised that a different approach needed to be taken. In recent growing seasons, seed has been inoculated with commercial fungi spores just prior to planting. While it is still too early to provide statistically robust outcomes and, bearing in mind that there are no “silver bullets” in agricultural production, the indications are that mycorrhizal fungi are promoting improvements in crop vitality, yield and soil condition [Johns 2014: 4].
Nitrogen: the double-edged sword, Jones 2014
The symbiosis between mycorrhizal fungi and plants drive carbon and nitrogen cycles. Fungi demand carbon exudate from plants in exchange for nitrogen and other nutrients retrieved and transported from the soil. The “liquid carbon” exuded from plant roots feeds mycorrhizal fungi and many other soil microbes, while also becoming stabilized in soil aggregates and humus. Jones explains that when this mycorrhizal exchange is inhibited by N fertilizer, which allows plants to absorb nitrogen “for free” (without providing liquid carbon in exchange), this reduces the flow of carbon into the soils, which in turn diminishes fungal networks and their delivery of micronutrients to plant hosts, and results in carbon-depleted soils.
Despite its abundance in the atmosphere, nitrogen is frequently the most limiting element for plants. There is a reason for this. Carbon, essential to photosynthesis and soil function, occurs as a trace gas, carbon dioxide, currently comprising 0.04% of the atmosphere. The most efficient way to transform CO2 to stable organic soil complexes (containing both C and N) is via the liquid carbon pathway. The requirement for biologically-fixed nitrogen drives this process.
If plants were able to access nitrogen directly from the atmosphere, their growth would be impeded by the absence of carbon-rich topsoil. We are witnessing an analogous situation in agriculture today. When inorganic nitrogen is provided, the supply of carbon to associative nitrogen fixing microbes is inhibited, resulting in carbon-depleted soils.
Reduced carbon flows impact a vast network of microbial communities, restricting the availability of essential minerals, trace elements, vitamins and hormones required for plant tolerance to environmental stresses such as frost and drought and resistance to insects and disease. Lowered micronutrient densities in plants also translate to reduced nutritional value of food [Jones 2014: 2-3].
Jones further explains how to modify agricultural practices to protect and build the soil: maintain year-round living ground cover, limit nitrogen and phosphorus fertilizer input, promote plant and microbial diversity, and integrate livestock into crop production systems.
Synthetic nitrogen fertilizers deplete soil nitrogen: a global dilemma for sustainable cereal production, Mulvaney 2009
There is a prevailing view that global food and ﬁber production will continue to expand because of modern agricultural management systems with improved cultivars and intensive chemical inputs dominated by synthetic ammoniacal fertilizers. The use of these fertilizers has led to concerns regarding water and air pollution but is generally perceived to play an essential role for sustaining agricultural productivity, not only by supplying the most important nutrient for cereal production but also by increasing the input of crop residues for building soil organic matter. The scientiﬁc soundness of the buildup concept has yet to be substantiated empirically using baseline data sets from long-term cropping experiments. The present paper and a companion study by Khan et al. (2007) provide many such data sets that encompass a variety of cereal cropping and management systems in diﬀerent parts of the world. Overwhelmingly, the evidence is diametrically opposed to the buildup concept and instead corroborates a view elaborated long ago by White (1927) and Albrecht (1938) that fertilizer N depletes soil organic matter by promoting microbial C utilization and N mineralization. An inexorable conclusion can be drawn: The scientiﬁc basis for input-intensive cereal production is seriously ﬂawed. The long-term consequences of continued reliance on current production practices will be a decline in soil productivity that increases the need for synthetic N fertilization, threatens food security, and exacerbates environmental degradation [Mulvaney 2009: 2308].
Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere, Paungfoo-Lonhienne 2015
In this study, nitrogen fertilization altered the relative abundance of fungal taxa in the rhizosphere, increasing fungal genera with known pathogenic traits, and decreasing a fungal phyla (Basidiomycetes) known to break down lignin, thus important for carbon cycling in the soil.
Fungi play important roles as decomposers, plant symbionts and pathogens in soils. The structure of fungal communities in the rhizosphere is the result of complex interactions among selection factors that may favour beneficial or detrimental relationships. Using culture-independent fungal community profiling, we have investigated the effects of nitrogen fertilizer dosage on fungal communities in soil and rhizosphere of field-grown sugarcane.The results show that the concentration of nitrogen fertilizer strongly modifies the composition but not the taxon richness of fungal communities in soil and rhizosphere. Increased nitrogen fertilizer dosage has a potential negative impact on carbon cycling in soil and promotes fungal genera with known pathogenic traits, uncovering a negative effect of intensive fertilization [Paungfoo-Lonhienne 2015:just 1].
Nitrogen fertilizer effects on soil carbon balances in Midwestern U.S. agricultural systems, Russell 2009
Despite increasing residue input in annual crop production systems, N fertilization does not increase soil organic carbon (SOC) over time because N fertilization also increases organic carbon (OC) decay. This study also shows that belowground OC inputs contribute to soil carbon sequestration more than aboveground OC inputs to the soil.
When all phases of the crop rotations were evaluated over the long term, OC decay rates increased concomitantly with OC input rates in several systems. Increases in decay rates with N fertilization apparently offset gains in carbon inputs to the soil in such a way that soil C sequestration was virtually nil in 78% of the systems studied, despite up to 48 years of N additions [Russell 2009: 1102].
Across all systems, SOC storage was signiﬁcantly correlated with the quantity of belowground OM [organic matter] inputs (P < 0.01, both sites). In contrast, SOC was not correlated with the quantity of aboveground inputs (P = 0.45, Nashua; P = 0.55, Kanawha) [Russell 2009: 1111].
This study highlights the importance of incorporating both production and decomposition processes, as well as the location (above- or below-ground) of detrital inputs into models of N-fertilization effects on soil C dynamics in agroecosystems. These results are highly relevant for evaluating the potential of N fertilization to mitigate the effects of removal of organic-matter ‘‘residue’’ from the system for bioenergy production. Our data suggest that the stimulation of OC decomposition by the addition of fertilizer N would likely counteract the positive effects of N fertilization on inputs of OC to the soil, at least for annual crops. Given the current quantity of N that is applied over such a large area, management strategies that can maintain high yields and also reduce N-fertilizer use would also have beneﬁcial environmental consequences. Our study indicates that selection of crops for higher belowground NPP [net primary production], in rotation with crops that ﬁx N, could maximize both yields and soil C sequestration without excessive N-fertilizer additions [Russell 2009: 1111].
Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil, Yao 2018
In this study, long-term phosphorus fertilization limited the extent to which the genes and proteins of microbial communities were allocated to degrading recalcitrant soil phytate to acquire phosphorus. In phosphorus-deficient soil, on the other hand, the genes responsible for breaking down recalcitrant substrate to acquire phosphorus were more prevalent in microbial communities. In other words, microbial communities can adapt genetically to different levels of nutrients in the soil in order to continue meeting their nutritional requirements. This adds to the body of evidence that fertilizer use impairs the inherent qualities of a living soil to nourish the plants growing there.
A greater than fourfold increase in the gene abundance of 3-phytase was the strongest response of soil communities to phosphorus deficiency. Phytase catalyses the release of phosphate from phytate, the most recalcitrant phosphorus-containing compound in soil organic matter. Genes and proteins for the degradation of phosphorus-containing nucleic acids and phospholipids, as well as the decomposition of labile carbon and nitrogen, were also enhanced in the phosphorus-deficient soils. In contrast, microbial communities in the phosphorus-rich soils showed increased gene abundances for the degradation of recalcitrant aromatic compounds, transformation of nitrogenous compounds and assimilation of sulfur. Overall, these results demonstrate the adaptive allocation of genes and proteins in soil microbial communities in response to shifting nutrient constraints [Yao 2018: 499].
In conclusion, our proteogenomics results provide systems biology insights into the adaptation of soil microbial communities to different levels of phosphorus availability in a humid tropical forest environment. Phosphorus deficiency significantly enhanced the genetic capabilities of microbial communities to extract phosphorus from phytate and, to a lesser extent, from nucleic acids and phospholipids. Long-term phosphorus fertilization altered the allocation of genes and proteins by microbial communities to acquire carbon, nitrogen and sulfur from a variety of substrates. The results suggest that the selective degradation of recalcitrant substrates, including phytate in phosphorus-deficient soils and aromatic compounds in phosphorus-rich soils, is an important means for microbial communities to balance their elemental requirements. The adaptive allocation of genes and proteins for acquisition of these nutrients in different soils can be explained as an optimal foraging strategy by which microbial communities maintain efficient growth under resource limitation [Yao 2018: 505].
Childers, Daniel L., et al., 2011, Sustainability challenges of phosphorus and food: solutions from closing the human phosphorus cycle, BioScience 61: 117–124, https://academic.oup.com/bioscience/article/61/2/117/242667
Elser, James & Elena Bennett, 2011, A broken biogeochemical cycle, Nature 478: 29-31, https://www.nature.com/articles/478029a
Johns, Christopher D., 2014, Agricultural Application of Mycorrhizal Fungi to Increase Crop Yields, Promote Soil Health and Combat Climate Change, published by Future Directions International, Nov. 18, 2014, http://futuredirections.org.au/wp-content/uploads/2014/11/FDI_Strategic_Analysis_Paper_-_Agricultural_Application_Of_Mycorrhizal_Fungi.pdf.
Jones, Christine, 2014, Nitrogen: the double-edged sword, retrieved on July 5, 2018 from http://www.amazingcarbon.com/PDF/JONES%20%27Nitrogen%27%20(21July14).pdf
Jongmans, A.G. et al., 1997, Rock-eating fungi, Nature 389: 682-683, https://www.nature.com/articles/39493
Leake, Jonathan et al., 2004, Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning, Can. J. Bot. 82: 1016–1045, http://www.nrcresearchpress.com/doi/abs/10.1139/b04-060#.W1vUIdJKiM8
Mulvaney R. L., S. A. Khan, & T. R. Ellsworth, 2009, Synthetic Nitrogen Fertilizers Deplete Soil Nitrogen: A Global Dilemma for Sustainable Cereal Production, Journal of Environmental Quality 38, 2295-2314: http://www.mudcitypress.com/PDF/mulvaney.pdf
Paungfoo-Lonhienne, Chanyarat, et al., 2015, Nitrogen fertilizer dose alters fungal communities in sugarcane soil and rhizosphere, Scientific Reports 5(8678), https://www.nature.com/articles/srep08678.
Russell, Ann E. et al, 2009, Nitrogen fertilizer effects on soil carbon balances in Midwestern U.S. agricultural systems, Ecological Applications 19(5), 1102-1113: https://esajournals.onlinelibrary.wiley.com/doi/10.1890/07-1919.1.
Schutz, Lukas et al., 2018, Meta-analysis of Biofertilizer Application in Agriculture, Frontiers in Plant Science 8, https://www.frontiersin.org/articles/10.3389/fpls.2017.02204/full.
Stevens, Bo Maxwell, et al., 2018, Mycorrhizal symbioses influence the trophic structure of the Serengeti, Journal of Ecology 106: 536-546, https://besjournals.onlinelibrary.wiley.com/doi/epdf/10.1111/1365-2745.12916
Stewart, B.A. & Rattan Lal, 2017, The nitrogen dilemma: Food or the environment, Journal of Soil and Water Conservation 72(6): 124A-128A, http://www.jswconline.org/content/72/6/124A.full.pdf+html?sid=ae515a44-e34a-4fa6-b549-06ebcc815d76
Yao, Qiuming, et al., 2018, Community proteogenomics reveals the systemic impact of phosphorus availability on microbial functions in tropical soil, Nature Ecology and Evolution 2: 499-509, https://www.nature.com/articles/s41559-017-0463-5