Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance
TL;DR: In this article, the authors evaluate competitive and mutualistic interactions between plants and microorganisms and analyse the ecological consequences of these interactions in the rhizosphere, and they find that despite strong competition between roots and micro-organisms for N, a temporal niche differentiation reflecting their generation times leads to mutualistic relationships in the root network.
Abstract: Demand of all living organisms on the same nutrients forms the basis for interspecific competition between plants and microorganisms in soils. This competition is especially strong in the rhizosphere. To evaluate competitive and mutualistic interactions between plants and microorganisms and to analyse ecological consequences of these interactions, we analysed 424 data pairs from 41 (15)N-labelling studies that investigated (15)N redistribution between roots and microorganisms. Calculated Michaelis-Menten kinetics based on K(m) (Michaelis constant) and V(max) (maximum uptake capacity) values from 77 studies on the uptake of nitrate, ammonia, and amino acids by roots and microorganisms clearly showed that, shortly after nitrogen (N) mobilization from soil organic matter and litter, microorganisms take up most N. Lower K(m) values of microorganisms suggest that they are especially efficient at low N concentrations, but can also acquire more N at higher N concentrations (V(max)) compared with roots. Because of the unidirectional flow of nutrients from soil to roots, plants are the winners for N acquisition in the long run. Therefore, despite strong competition between roots and microorganisms for N, a temporal niche differentiation reflecting their generation times leads to mutualistic relationships in the rhizosphere. This temporal niche differentiation is highly relevant ecologically because it: protects ecosystems from N losses by leaching during periods of slow or no root uptake; continuously provides roots with available N according to plant demand; and contributes to the evolutionary development of mutualistic interactions between roots and microorganisms.
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TL;DR: It is suggested that, irrespective of their volume, the hotspots are mainly responsible for the ecologically relevant processes in soil, including succession in microbial communities and intense intra- and interspecific competition affecting C use efficiency, microbial growth and turnover.
Abstract: Soils are the most heterogeneous parts of the biosphere, with an extremely high differentiation of properties and processes within nano- to macroscales. The spatial and temporal heterogeneity of input of labile organics by plants creates microbial hotspots over short periods of time – the hot moments. We define microbial hotspots as small soil volumes with much faster process rates and much more intensive interactions compared to the average soil conditions. Such hotspots are found in the rhizosphere, detritusphere, biopores (including drilosphere) and on aggregate surfaces, but hotspots are frequently of mixed origin. Hot moments are short-term events or sequences of events inducing accelerated process rates as compared to the average rates. Thus, hotspots and hot moments are defined by dynamic characteristics, i.e. by process rates. For this hotspot concept we extensively reviewed and examined the localization and size of hotspots, spatial distribution and visualization approaches, transport of labile C to and from hotspots, lifetime and process intensities, with a special focus on process rates and microbial activities. The fraction of active microorganisms in hotspots is 2–20 times higher than in the bulk soil, and their specific activities (i.e. respiration, microbial growth, mineralization potential, enzyme activities, RNA/DNA ratio) may also be much higher. The duration of hot moments in the rhizosphere is limited and is controlled by the length of the input of labile organics. It can last a few hours up to a few days. In the detritusphere, however, the duration of hot moments is regulated by the output – by decomposition rates of litter – and lasts for weeks and months. Hot moments induce succession in microbial communities and intense intra- and interspecific competition affecting C use efficiency, microbial growth and turnover. The faster turnover and lower C use efficiency in hotspots counterbalances the high C inputs, leading to the absence of strong increases in C stocks. Consequently, the intensification of fluxes is much stronger than the increase of pools. Maintenance of stoichiometric ratios by accelerated microbial growth in hotspots requires additional nutrients (e.g. N and P), causing their microbial mining from soil organic matter, i.e. priming effects. Consequently, priming effects are localized in microbial hotspots and are consequences of hot moments. We estimated the contribution of the hotspots to the whole soil profile and suggested that, irrespective of their volume, the hotspots are mainly responsible for the ecologically relevant processes in soil. By this review, we raised the importance of concepts and ecological theory of distribution and functioning of microorganisms in soil.
1,084 citations
TL;DR: This review focuses on the interaction of plants and root associated bacteria enhancing plant mineral nutrition, summarizing the current knowledge in several research fields that can converge to improve the understanding of the molecular mechanisms underpinning this phenomenon.
Abstract: In their natural environment plants are part of a rich ecosystem including numerous and diverse microorganisms in the soil. It has been long recognized that some of these microbes, such as mycorrhizal fungi or nitrogen fixing symbiotic bacteria, play important roles in plant performance by improving mineral nutrition. However, the full range of microbes associated with plants and their potential to replace synthetic agricultural inputs has only recently started to be uncovered. In the last few years a great progress has been made in the knowledge on composition of rhizospheric microbiomes and their dynamics. There is clear evidence that plants shape microbiome structures, most probably by root exudates, and also that bacteria have developed various adaptations to thrive in the rhizospheric niche. The mechanisms of these interactions and the processes driving the alterations in microbiomes are however largely unknown. In this review we focus on the interaction of plants and root associated bacteria enhancing plant mineral nutrition, summarizing the current knowledge in several research fields that can converge to improve our understanding of the molecular mechanisms underpinning this phenomenon.
748 citations
TL;DR: Wang et al. as mentioned in this paper used extensive datasets that include both wet and dry N deposition to evaluate the spatiotemporal variation of N deposition and the changes of its components in China during 1980-2015.
Abstract: Increasing atmospheric nitrogen deposition can influence food production, environmental quality and climate change from the regional to global scales. As the largest developing country, China is expected to experience a rapid increase in N deposition. However, the lack of information on dry N deposition limits our understanding of the historical trend of the total N deposition, as well as the main drivers of this trend. Here, we use extensive datasets that include both wet and dry N deposition to evaluate the spatiotemporal variation of N deposition and the changes of its components in China during 1980–2015. Three significant transitions in N deposition in China were observed. First, the total N deposition began to stabilize in 2001–2005, mostly due to a decline in wet NH4+ deposition. Subsequently, a shift to approximately equal wet and dry N deposition occurred in 2011–2015, accompanied by increasing dry deposition. Finally, the contribution of reduced N components in the deposition decreased due to increasing NO3− deposition. These transitions were jointly driven by changes in the socioeconomic structure in China and vigorous controls in N pollution. The three observed important transitions challenge the traditional views about the continuous increase in N deposition in China. Nitrogen deposition in China has been almost constant over the past decade, as decreasing wet deposition has balanced increasing dry deposition, according to analyses of extensive datasets on wet and dry nitrogen depositions in China.
424 citations
TL;DR: The importance of NF bacteria and P solubilizing/mobilizing microbes as well as their interactions with mineral P fertilization in improving crop productivity and fertilizers efficiency and positive consequences on plant mineral uptake, crop productivity, and resiliency to environmental constraints are reported.
Abstract: Tomorrow’s agriculture, challenged by increasing global demand for food, scarcity of arable lands, and resources alongside multiple environment pressures, needs to be managed smartly through sustainable and eco-efficient approaches. Modern agriculture has to be more productive, sustainable and environmentally friendly. While macronutrients such as nitrogen (N), phosphorus (P), potassium (K) and sulfur (S) supplied by mineral fertilizers are vital to crop production, agriculturally beneficial microorganisms may also contribute directly (i.e. biological N2 fixation, P solubilization, phytohormone production, etc.) or indirectly (i.e. antimicrobial compounds biosynthesis, elicitation of induced systemic resistance, etc.) to crop improvement and fertilizers efficiency. Microbial-based bioformulations that increase plant performance are greatly needed, and in particular bioformulations that exhibit complementary and synergistic effects with mineral fertilization. Such an integrated soil fertility management strategy has been demonstrated through several controlled and non-controlled experiments, but more efforts have to be made in order to thoroughly understand the multiple functions of beneficial microbes’ functions within the soil microbial community itself and in interaction with plants and mineral resources. In fact, the combined usage of microbial (i.e. beneficial microorganisms: N2-fixing (NF), P-solubilizing and P mobilizing, etc.) and mineral resources is an emerging research area that aims to design and develop efficient microbial formulations which are highly compatible with mineral inputs, with positive impacts on both crops and environment. This novel approach is likely to be of a global interest, especially in most N- and P-deficient agro-ecosystems. In this review, we report on the importance of NF bacteria and P solubilizing/mobilizing microbes as well as their interactions with mineral P fertilization in improving crop productivity and fertilizers efficiency. In addition, we shed light on the interactive and synergistic effects that may occur within multi-trophic interactions involving those two microbial groups and positive consequences on plant mineral uptake, crop productivity and resiliency to environmental constraints. Improving use of mineral nutrients is a must to securing higher yield and productivity in a sustainable manner, therefore continuously designing, developing and testing innovative integrated plant nutrient management systems based on relevant biological resources (crops and microorganisms) is highly required.
315 citations
TL;DR: Investigating the RPE of two plant species grown in two soil types and sampled at two phenological stages over an 88-day period shows that root–soil–microbial interactions can stimulate soil C and N mineralization through rhizosphere effects, providing clear evidence for the microbial activation hypothesis of RPE.
Abstract: Living roots and their rhizodeposits affect microbial activity and soil carbon (C) and nitrogen (N) mineralization. This so-called rhizosphere priming effect (RPE) has been increasingly recognized recently. However, the magnitude of the RPE and its driving mechanisms remain elusive. Here we investigated the RPE of two plant species (soybean and sunflower) grown in two soil types (a farm or a prairie soil) and sampled at two phenological stages (vegetative and mature stages) over an 88-day period in a greenhouse experiment. We measured soil C mineralization using a continuous 13C-labeling method, and quantified gross N mineralization with a 15N-pool dilution technique. We found that living roots significantly enhanced soil C mineralization, by 27–245%. This positive RPE on soil C mineralization did not vary between the two soils or the two phenological stages, but was significantly greater in sunflower compared to soybean. The magnitude of the RPE was positively correlated with rhizosphere respiration rate across all treatments, suggesting the variation of RPE among treatments was likely caused by variations in root activity and rhizodeposit quantity. Moreover, living roots stimulated gross N mineralization rate by 36–62% in five treatments, while they had no significant impact in the other three treatments. We also quantified soil microbial biomass and extracellular enzyme activity when plants were at the vegetative stage. Generally, living roots increased microbial biomass carbon by 0–28%, β-glucosidase activity by 19–56%, and oxidative enzyme activity by 0–46%. These results are consistent with the positive rhizosphere effect on soil C (45–79%) and N (10–52%) mineralization measured at the same period. We also found significant positive relationships between β-glucosidase activity and soil C mineralization rates and between oxidative enzyme activity and gross N mineralization rates across treatments. These relationships provide clear evidence for the microbial activation hypothesis of RPE. Our results demonstrate that root–soil–microbial interactions can stimulate soil C and N mineralization through rhizosphere effects. The relationships between the RPE and rhizosphere respiration rate and soil enzyme activity can be used for explicit representations of RPE in soil organic matter models.
293 citations
References
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Book•
01 Jan 1982
TL;DR: In this article, the Soil as a Plant Nutrient Medium is discussed and the importance of water relations in plant growth and crop production, and the role of water as a plant nutrient medium.
Abstract: 1. Plant Nutrients. 2. The Soil as a Plant Nutrient Medium. 3. Nutrient Uptake and Assimilation. 4. Plant Water Relationships. 5. Plant Growth and Crop Production. 6. Fertilizer Application. 7. Nitrogen. 8. Sulphur. 9. Phosphorus. 10. Potassium. 11. Calcium. 12. Magnesium. 13. Iron. 14. Manganese. 15. Zinc. 16. Copper. 17. Molybdenum. 18. Boron. 19. Further Elements of Importance. 20. Elements with More Toxic Effects. General Readings. References. Index.
4,130 citations
TL;DR: The results suggest that the global N and C cycles interact strongly and that geography can mediate ecosystem response to N within certain biome types.
Abstract: Our meta-analysis of 126 nitrogen addition experiments evaluated nitrogen (N) limitation of net primary production (NPP) in terrestrial ecosystems. We tested the hypothesis that N limitation is widespread among biomes and influenced by geography and climate. We used the response ratio (R approximately equal ANPP(N)/ANPP(ctrl)) of aboveground plant growth in fertilized to control plots and found that most ecosystems are nitrogen limited with an average 29% growth response to nitrogen (i.e., R = 1.29). The response ratio was significant within temperate forests (R = 1.19), tropical forests (R = 1.60), temperate grasslands (R = 1.53), tropical grasslands (R = 1.26), wetlands (R = 1.16), and tundra (R = 1.35), but not deserts. Eight tropical forest studies had been conducted on very young volcanic soils in Hawaii, and this subgroup was strongly N limited (R = 2.13), which resulted in a negative correlation between forest R and latitude. The degree of N limitation in the remainder of the tropical forest studies (R = 1.20) was comparable to that of temperate forests, and when the young Hawaiian subgroup was excluded, forest R did not vary with latitude. Grassland response increased with latitude, but was independent of temperature and precipitation. These results suggest that the global N and C cycles interact strongly and that geography can mediate ecosystem response to N within certain biome types.
2,130 citations
TL;DR: A complete new conceptual model of the soil N cycle needs to incorporate recent research on plant–microbe competition and microsite processes to explain the dynamics of N across the wide range of N availability found in terrestrial ecosystems.
Abstract: Until recently, the common view of the terrestrial nitrogen cycle had been driven by two core assumptions—plants use only inorganic N and they compete poorly against soil microbes for N. Thus, plants were thought to use N that microbes “left over,” allowing the N cycle to be divided cleanly into two pieces—the microbial decomposition side and the plant uptake and use side. These were linked by the process of net mineralization. Over the last decade, research has changed these views. N cycling is now seen as being driven by the depolymerization of N-containing polymers by microbial (including mycorrhizal) extracellular enzymes. This releases organic N-containing monomers that may be used by either plants or microbes. However, a complete new conceptual model of the soil N cycle needs to incorporate recent research on plant–microbe competition and microsite processes to explain the dynamics of N across the wide range of N availability found in terrestrial ecosystems. We discuss the evolution of thinking abou...
2,126 citations
Book•
12 Nov 1998
TL;DR: In this article, basic Soil-Plant Relationships are discussed, and the authors present an overview of the current state of the art in terms of agricultural productivity and environmental quality.
Abstract: 1. Introduction. 2. Basic Soil-Plant Relationships. 3. Soil Acidity and Alkalinity. 4. Nitrogen. 5. Phosphorus. 6. Potassium. 7. Sulfur, Calcium, and Magnesium. 8. Micronutrients. 9. Soil Fertility Evaluation. 10. Basics of Nutrient Management. 11. Nutrients, Water Use, and Other Interactions. 12. Economics of Plant-Nutrient Use. 13. Agricultural Productivity and Environmental Quality. Index.
1,929 citations
TL;DR: In this paper, a review of the literature on well-constrained carbon:nitrogen:phosphorus (C:N:P) ratios in planktonic biomass has motivated ecologists to search for similar patterns in terrestrial ecosystems.
Abstract: Well-constrained carbon:nitrogen:phosphorus (C:N:P) ratios in planktonic biomass, and their importance in advancing our understanding of biological processes and nutrient cycling in marine ecosystems, has motivated ecologists to search for similar patterns in terrestrial ecosystems. Recent analyses indicate the existence of “Redfield-like” ratios in plants, and such data may provide insight into the nature of nutrient limitation in terrestrial ecosystems. We searched for analogous patterns in the soil and the soil microbial biomass by conducting a review of the literature. Although soil is characterized by high biological diversity, structural complexity and spatial heterogeneity, we found remarkably consistent C:N:P ratios in both total soil pools and the soil microbial biomass. Our analysis indicates that, similar to marine phytoplankton, element concentrations of individual phylogenetic groups within the soil microbial community may vary, but on average, atomic C:N:P ratios in both the soil (186:13:1) and the soil microbial biomass (60:7:1) are well-constrained at the global scale. We did see significant variation in soil and microbial element ratios between vegetation types (i.e., forest versus grassland), but in most cases, the similarities in soil and microbial element ratios among sites and across large scales were more apparent than the differences. Consistent microbial biomass element ratios, combined with data linking specific patterns of microbial element stoichiometry with direct evidence of microbial nutrient limitation, suggest that measuring the proportions of C, N and P in the microbial biomass may represent another useful tool for assessing nutrient limitation of ecosystem processes in terrestrial ecosystems.
1,704 citations