Nutrient Acquisition Strategies Research Articles

Ecophysiological Performance of Proteaceae Species From Southern South America Growing on Substrates Derived From Young Volcanic Materials.

Southern South American Proteaceae thrive on young volcanic substrates, which are extremely low in plant-available phosphorus (P). Most Proteaceae exhibit a nutrient-acquisition strategy based on the release of carboxylates from specialized roots, named cluster roots (CR). Some Proteaceae colonize young volcanic substrates which has been related to CR functioning. However, physiological functioning of other Proteaceae on recent volcanic substrates is unknown. We conducted an experiment with seedlings of five Proteaceae (Gevuina avellana, Embothrium coccineum, Lomatia hirsuta, L. ferruginea, and L. dentata) grown in three volcanic materials. Two of them are substrates with very low nutrient concentrations, collected from the most recent deposits of the volcanoes Choshuenco and Calbuco (Chile). The other volcanic material corresponds to a developed soil that exhibits a high nutrient availability. We assessed morphological responses (i.e., height, biomass, and CR formation), seed and leaf macronutrient and micronutrient concentrations and carboxylates exuded by roots. The results show that G. avellana was less affected by nutrient availability of the volcanic substrate, probably because it had a greater nutrient content in its seeds and produced large CR exuding carboxylates that supported their initial growth. Embothrium coccineum exhibited greater total plant height and leaf P concentration than Lomatia species. In general, in all species leaf macronutrient concentrations were reduced on nutrient-poor volcanic substrates, while leaf micronutrient concentrations were highly variable depending on species and volcanic material. We conclude that Proteaceae from temperate rainforests differ in their capacity to grow and acquire nutrients from young and nutrient-poor volcanic substrates. The greater seed nutrient content, low nutrient requirements (only for G. avellana) and ability to mobilize nutrients help explain why G. avellana and E. coccineum are better colonizers of recent volcanic substrates than Lomatia species.

Enzyme stoichiometry evidence revealed that five years nitrogen addition exacerbated the carbon and phosphorus limitation of soil microorganisms in a Phyllostachys pubescens forest.

The activity and stoichiometry of soil extracellular enzyme can provide a good indication for changes in soil nutrient availability and microbial demands for nutrients. However, it remains unclear how would nitrogen (N) deposition affect nutrient limitation of microbes in subtropical forest soils. We conducted a 5 years N addition experiment in a subtropical Phyllostachys pubescens forest. The soil nutrients and enzyme activities associated with carbon (C), N, and phosphorus (P) cycles were measured. We also examined the nutrient distribution of microorganisms using enzyme stoichiometry and vector analysis. The results showed that N addition significantly decreased the contents of soil soluble organic C and available P and increased that of available N. Furthermore, N addition significantly decreased β-N-acetyl-glucosaminidase (NAG) activity and NAG/ microbial biomass carbon (MBC), and increased acid phosphatase (ACP) and ACP/MBC. The low and moderate N addition levels significantly increased enzyme C/P, vector length, and vector angle, but significantly decreased enzyme N/P. Results of redundancy analysis showed that the change in soil enzyme activity and enzymatic stoichiometry were mainly driven by soil available P content under N addition. In summary, N addition altered the microbial nutrient acquisition strategy, which increased nutrient allocation to P-acquiring enzyme production but reduced that to N-acquiring enzyme production. Moreover, N addition exacerbated the C and P limitation of soil microorganisms. Appropriate amount of P fertilizer could be applied to improve soil fertility of subtropical P. pubescens forest in the future.

The enigma of environmental pH sensing in plants.

Environmental pH is a critical parameter for innumerable chemical reactions, myriad biological processes and all forms of life. The mechanisms that underlie the perception of external pH (pHe) have been elucidated in detail for bacteria, fungi and mammalian cells; however, little information is available on whether and, if so, how pHe is perceived by plants. This is particularly surprising since hydrogen ion activity of the substrate is of paramount significance for plants, governing the availability of mineral nutrients, the structure of the soil microbiome and the composition of natural plant communities. Rapid changes in soil pH require constant readjustment of nutrient acquisition strategies, which is associated with dynamic alterations in gene expression. Referring to observations made in diverse experimental set-ups that unambiguously show that pHe per se affects gene expression, we hypothesize that sensing of pHe in plants is mandatory to prioritize responses to various simultaneously received environmental cues.

Rapid responses of root traits and productivity to phosphorus and cation additions in a tropical lowland forest in Amazonia.

Soil nutrient availability can strongly affect root traits. In tropical forests, phosphorus (P) is often considered the main limiting nutrient for plants. However, support for the P paradigm is limited, and N and cations might also control tropical forests functioning. We used a large-scale experiment to determine how the factorial addition of nitrogen (N), P and cations affected root productivity and traits related to nutrient acquisition strategies (morphological traits, phosphatase activity, arbuscular mycorrhizal colonisation and nutrient contents) in a primary rainforest growing on low-fertility soils in Central Amazonia after 1 yr of fertilisation. Multiple root traits and productivity were affected. Phosphorus additions increased annual root productivity and root diameter, but decreased root phosphatase activity. Cation additions increased root productivity at certain times of year, also increasing root diameter and mycorrhizal colonisation. P and cation additions increased their element concentrations in root tissues. No responses were detected with N addition. Here we showed that rock-derived nutrients determined root functioning in low-fertility Amazonian soils, demonstrating not only the hypothesised importance of P, but also highlighting the role of cations. The changes in fine root traits and productivity indicated that even slow-growing tropical rainforests can respond rapidly to changes in resource availability.

Correction to: Towards a trait-based understanding of Symbiodiniaceae nutrient acquisition strategies

This erratum is published as panels of Fig. 2 were missing with the proper letters as per original submission and should be displayed as (Fig. 2).

Quantifying fluorescent glycan uptake to elucidate strain-level variability in foraging behaviors of rumen bacteria

Gut microbiomes, such as the microbial community that colonizes the rumen, have vast catabolic potential and play a vital role in host health and nutrition. By expanding our understanding of metabolic pathways in these ecosystems, we will garner foundational information for manipulating microbiome structure and function to influence host physiology. Currently, our knowledge of metabolic pathways relies heavily on inferences derived from metagenomics or culturing bacteria in vitro. However, novel approaches targeting specific cell physiologies can illuminate the functional potential encoded within microbial (meta)genomes to provide accurate assessments of metabolic abilities. Using fluorescently labeled polysaccharides, we visualized carbohydrate metabolism performed by single bacterial cells in a complex rumen sample, enabling a rapid assessment of their metabolic phenotype. Specifically, we identified bovine-adapted strains of Bacteroides thetaiotaomicron that metabolized yeast mannan in the rumen microbiome ex vivo and discerned the mechanistic differences between two distinct carbohydrate foraging behaviors, referred to as “medium grower” and “high grower.” Using comparative whole-genome sequencing, RNA-seq, and carbohydrate-active enzyme fingerprinting, we could elucidate the strain-level variability in carbohydrate utilization systems of the two foraging behaviors to help predict individual strategies of nutrient acquisition. Here, we present a multi-faceted study using complimentary next-generation physiology and “omics” approaches to characterize microbial adaptation to a prebiotic in the rumen ecosystem.49JS9nbEEXk7bV4NZX-91MVideo abstract

Contribution of root traits to variations in soil microbial biomass and community composition

It is well known that plant root-microbe interactions are critical drivers of ecosystem processes such as soil carbon and nutrient cycling; however, considerable uncertainties exist about how root chemical and morphological traits influence soil microbial community composition. We used 13 tree species grown in field monocultures in subtropical China to explore the ecological linkages between leaves, leaf litter, and root chemical and morphological traits associated with plant growth and nutrient-acquisition strategies, as well as soil microbial biomass, the fungi to bacteria (F/B) ratio, and Gram-positive to Gram-negative bacteria (GP/GN) ratio. The combination of above- and belowground traits captured a greater proportion of variations in soil microbial biomass and community composition than did aboveground traits alone. Individually, root traits explained more variations of the F/B and GP/GN ratios than did the individual effects of aboveground leaf or leaf litter traits. All distinct microbial biomass groups and F/B ratios decreased with the specific root length, whereas the F/B ratio increased, and the GP/GN ratio decreased with root tissue density. Our study highlighted the importance of the functional traits of plant roots in determining the microbial biomass and community composition in forest ecosystems. The combination of leaf and root traits may improve our understanding of the mechanisms that underly plant-microbe interactions toward the sustainable management of forest ecosystems.

Root positioning and trait shifts in Hibbertia racemosa as dependent on its neighbour's nutrient-acquisition strategy.

Nutrient-poor ecosystems globally exhibit high plant diversity. One mechanism enabling the co-existence of species in such ecosystems is facilitation among plants with contrasting nutrient-acquisition strategies. The ecophysiological processes underlying these interactions remain poorly understood. We hypothesized that root positioning plays a role between sympatric species in nutrient-poor vegetation. We investigated how the growth traits of the focal mycorrhizal non-cluster-rooted Hibbertia racemosa change when grown in proximity of non-mycorrhizal Banksia attenuata, which produces cluster roots that increase nutrient availability, compared with growth with conspecifics. Focal plants were placed in the centre of rhizoboxes, and biomass allocation, root system architecture, specific root length (SRL), and leaf nutrient concentration were assessed. When grown with B. attenuata, focal plants decreased root investment, increased root growth towards B. attenuata, and positioned their roots near B. attenuata cluster roots. SRL was greater, and the degree of localized root investment correlated positively with B. attenuata cluster-root biomass. Total nutrient contents in the focal individuals were greater when grown with B. attenuata. Focal plants directed their root growth towards the putatively facilitating neighbour's cluster roots, modifying root traits and investment. Preferential root positioning and root morphological traits play important roles in positive plant-plant interactions.

Towards a trait-based understanding of Symbiodiniaceae nutrient acquisition strategies

Symbiodiniaceae is a diverse group of dinoflagellates that form symbioses with marine invertebrates, provisioning energy and nutrients for their hosts. Symbiont diversity is a well-known predictor of host fitness and stress tolerance. Yet, we have a limited understanding of the mechanisms by which in hospite symbiont communities are structured. Therefore, we hypothesized that phylogenetic differences in nitrogen assimilation may affect symbiont dominance, as has been demonstrated in phytoplankton communities. Here, we quantified species-specific rates of nitrate assimilation using stable isotope labeling, and investigated key traits that have been adopted in phytoplankton ecology to explain the fundamental concept of nitrogen acquisition strategies and size-related trade-offs in Symbiodiniaceae. Traits related to structure and function were measured to look for convergent ecological strategies. Despite the limited sample size, we could distinguish two groups among the five species of Symbiodiniaceae with features described by the phytoplankton’s competition theories for resources: the affinity-adapted species which were associated with larger size, higher nitrogen content and nitrate affinity; and the velocity-adapted species which were small size, efficient in maximum nitrate assimilation, specific carbon assimilation rate, and growth. Our work supports the relevance of a functional trait-based approach to describe Symbiodinaceae diversity. The two contrasting nitrogen acquisition strategies identified may be fundamental to explain the composition and dynamics of Symbiodinaceae in hospite, stressing the importance of bottom-up mechanisms in shaping symbiont composition.

Carbon sequestration: counterintuitive feedback of plant growth

Interaction between the atmosphere, plants and soils plays an important role in the carbon cycle. Soils contain vast amounts of carbon, but their capacity to keep it belowground depends on the long-term ecosystem dynamics. Plant growth has the potential of adding or releasing carbon from soil stocks. Since plant growth is also stimulated by higher CO2 levels, understanding its impact on soils becomes crucial for estimating carbon sequestration at the ecosystem level. A recent meta-analysis explored the effect CO2 levels have in plant versus soil carbon sequestration. The integration of 108 experiments performed across different environments revealed that the magnitude of plant growth and the nutrient acquisition strategy result in counterintuitive feedback for soil carbon sequestration.

Temporal trends of plant nutrient-acquisition strategies with soil age and their ecological significance

Temporal trends of plant nutrient-acquisition strategies with soil age and their ecological significance

Sugar Beet Shoot and Root Phenotypic Plasticity to Nitrogen, Phosphorus, Potassium and Lime Omission

In low input agriculture, a thorough understanding of the plant-nutrient interactions plays a central role. This study aims to investigate the effects of nitrogen (N), phosphorus (P), and potassium (K) and liming omission on shoot growth as well as on topsoil root biomass, growth and morphology (tuber and fibrous roots) of sugar beet grown under field conditions at the Dikopshof long-term fertilizer experiment (Germany). Classical shoot observation methods were combined with root morphology and link measurements using an image analysis program. Omission of the nutrients N, P and K as well as of liming led to a significant decrease in shoot growth. Tuber yield was lowest for the unfertilized and the K omission treatment. The root shoot ratio was highest in the N deficient treatment. In the K omission treatment, a strategic change from a less herringbone root type (early stage) to a more herringbone root type (late stage), which is more efficient for the acquisition of mobile nutrients, was observed. By contrast, a change from a more herringbone (early stage) to a less herringbone root type (late stage) which is less expensive to produce and maintain was observed in the unfertilized treatment. We conclude that sugar beet alters its root morphology as a nutrient acquisition strategy.

Impacts of Arctic Shrubs on Root Traits and Belowground Nutrient Cycles Across a Northern Alaskan Climate Gradient.

Deciduous shrubs are expanding across the graminoid-dominated nutrient-poor arctic tundra. Absorptive root traits of shrubs are key determinants of nutrient acquisition strategy from tundra soils, but the variations of shrub root traits within and among common shrub genera across the arctic climatic gradient are not well resolved. Consequently, the impacts of arctic shrub expansion on belowground nutrient cycling remain largely unclear. Here, we collected roots from 170 plots of three commonly distributed shrub genera (Alnus, Betula, and Salix) and a widespread sedge (Eriophorum vaginatum) along a climatic gradient in northern Alaska. Absorptive root traits that are relevant to the strategy of plant nutrient acquisition were determined. The influence of aboveground dominant vegetation cover on the standing root biomass, root productivity, vertical rooting profile, as well as the soil nitrogen (N) pool in the active soil layer was examined. We found consistent root trait variation among arctic plant genera along the sampling transect. Alnus and Betula had relatively thicker and less branched, but more frequently ectomycorrhizal colonized absorptive roots than Salix, suggesting complementarity between root efficiency and ectomycorrhizal dependence among the co-existing shrubs. Shrub-dominated plots tended to have more productive absorptive roots than sedge-dominated plots. At the northern sites, deep absorptive roots (>20 cm depth) were more frequent in birch-dominated plots. We also found shrub roots extensively proliferated into the adjacent sedge-dominated plots. The soil N pool in the active layer generally decreased from south to north but did not vary among plots dominated by different shrub or sedge genera. Our results reveal diverse nutrient acquisition strategies and belowground impacts among different arctic shrubs, suggesting that further identifying the specific shrub genera in the tundra landscape will ultimately provide better predictions of belowground dynamics across the changing arctic.

Contrasting phosphorus sensitivity of two Australian native monocots adapted to different habitats

Contrasting nutrient-acquisition strategies would explain why species differ in their distribution in relation to soil phosphorus (P) availability, promoting diversity. However, what drives the differential distribution of plant species with the same P-acquisition strategy remains poorly understood. We selected two Haemodoraceae species, Anigozanthos flavidus and Macropidia fuliginosa, to investigate physiological responses in non-mycorrhizal monocots adapted to different edaphic habitats that vary in P availability. Plants were grown in nutrient solution in large tanks at a range of P concentrations (0, 0.1, 1, 10 µM P). After seven months, we measured growth, photosynthetic rate, net P-uptake capacity, and leaf [P]. Fresh weights of A. flavidus plants were highest at 1 µM P and lowest at 0 µM P. Fresh weights of M. fuliginosa plants were lowest at 10 µM P compared with those at other P levels. Rates of P uptake by A. flavidus showed a steady decline with increasing P level during growth from 0 to 1 µM P, and then a sharp decline from 1 to 10 µM P. Rates of P uptake in M. fuliginosa did not differ among growth P levels, except between 0 and 1 µM P. Both species showed a drastic increase in the concentration of both total P and inorganic P at 10 µM P. The results support our hypothesis that A. flavidus is efficient in down-regulating its P-uptake capacity, while M. fuliginosa is not. Thus, partly explaining the narrower and wider distribution of these species.

Biotic interactions with mycorrhizal systems as extended nutrient acquisition strategies shaping forest soil communities and functions

Plant nutrient acquisition strategies involving ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) associations, are key plant functional traits leading to distinct carbon (C) and nutrient dynamics in forests. Yet, little is known about how these strategies influence the structure and functioning of soil communities, and if such mycorrhizal effects may be more or less pronounced depending on the type of forest and various abiotic factors. Here we explore the potential interactions occurring between plant-EcM and plant-AM systems with the diverse soil organisms occurring in forest soils, and in the process draw attention to major issues that are worthy for future research directions. Based on these potential interactions, we suggest that EcM systems, especially those involving gymnosperms in colder climates, may select for a soil community with a narrow set of functions. These EcM systems may exhibit low functional redundancy, dominated by symbiotic interactions, where EcM fungi maintain low pH and high C/N conditions in order to tightly control nutrient cycling and maintain the dominance of EcM trees. By contrast, AM systems, particularly those involving deciduous angiosperm trees in mild and warmer climates, may facilitate a functionally more diverse and redundant soil community tending towards the dominance of competitive and antagonistic interactions, but also with a range of symbiotic interactions that together maintain diverse plant communities. We propose that the contrasting belowground interactions in AM and EcM systems act as extended nutrient acquisition traits that contribute greatly to the prevailing nutrient and C dynamics occurring in these systems.

Yap/Taz promote the scavenging of extracellular nutrients through macropinocytosis.

The uptake of macromolecules and cellular debris through macropinocytosis has emerged as an important nutrient acquisition strategy of cancer cells. Genetic alterations commonly found in human cancers (e.g. mutations in KRAS or loss of PTEN) have been shown to increase macropinocytosis. To identify additional effectors that enable cell growth dependent on the uptake of extracellular proteins, pancreatic ductal adenocarcinoma (PDA) cells were selected for growth in medium where extracellular albumin was the obligate source of the essential amino acid leucine. Analysis of global changes in chromatin availability and gene expression revealed that PDA cells selected under these conditions exhibited elevated activity of the transcriptional activators Yap/Taz. Knockout of Yap/Taz prevented growth of PDA cells in leucine-deficient medium, but not in complete medium. Furthermore, constitutively active forms of Yap or Taz were sufficient to stimulate macropinocytosis of extracellular protein. In addition to promoting the uptake of plasma proteins, Yap/Taz also promoted the scavenging of apoptotic cell bodies and necrotic debris by PDA cells. The Yap/Taz transcriptional target Axl was found to be essential for cell growth dependent on the uptake of dead cells and cell debris. Together, these studies suggest that the Hippo pathway effectors Yap and Taz are important transcriptional regulators of endocytic nutrient uptake.

Mean annual temperature influences local fine root proliferation and arbuscular mycorrhizal colonization in a tropical wet forest.

Mean annual temperature (MAT) is an influential climate factor affecting the bioavailability of growth‐limiting nutrients nitrogen (N) and phosphorus (P). In tropical montane wet forests, warmer MAT drives higher N bioavailability, while patterns of P availability are inconsistent across MAT. Two important nutrient acquisition strategies, fine root proliferation into bulk soil and root association with arbuscular mycorrhizal fungi, are dependent on C availability to the plant via primary production. The case study presented here tests whether variation in bulk soil N bioavailability across a tropical montane wet forest elevation gradient (5.2°C MAT range) influences (a) morphology fine root proliferation into soil patches with elevated N, P, and N+P relative to background soil and (b) arbuscular mycorrhizal fungal (AMF) colonization of fine roots in patches. We created a fully factorial fertilized root ingrowth core design (N, P, N+P, unfertilized control) representing soil patches with elevated N and P bioavailability relative to background bulk soil. Our results show that percent AMF colonization of roots increased with MAT (r 2 = .19, p = .004), but did not respond to fertilization treatments. Fine root length (FRL), a proxy for root foraging, increased with MAT in N+P‐fertilized patches only (p = .02), while other fine root morphological parameters did not respond to the gradient or fertilized patches. We conclude that in N‐rich, fine root elongation into areas with elevated N and P declines while AMF abundance increases with MAT. These results indicate a tradeoff between P acquisition strategies occurring with changing N bioavailability, which may be influenced by higher C availability with warmer MAT.

Variations in the natural 13C and 15N abundance of plants and soils under long-term N addition and precipitation reduction: interpretation of C and N dynamics

BackgroundThe nitrogen isotope natural abundance (δ15N) provides integrated information on ecosystem N dynamics, and carbon isotope natural abundance (δ13C) has been used to infer how water-using processes of plants change in terrestrial ecosystems. However, how δ13C and δ15N abundances in plant life and soils respond to N addition and water availability change is still unclear. Thus, δ13C and δ15N abundances in plant life and soils were used to investigate the effects of long-time (10 years) N addition (+ 50 kg N·ha− 1·yr− 1) and precipitation reduction (− 30% of throughfall) in forest C and N cycling traits in a temperate forest in northern China.ResultsWe analyzed the δ13C and δ15N values of dominant plant foliage, litterfall, fungal sporophores, roots, and soils in the study. The results showed that δ15N values of foliage, litterfall, and surface soil layer’s (0–10 cm) total N were significantly increased by N addition, while δ15N values of fine roots and coarse roots were considerably decreased. Nitrogen addition also significantly increased the δ13C value of fine roots and total N concentration of the surface soil layer compared with the control. The C concentration, δ13C, and δ15N values of foliage and δ15N values of fine roots were significantly increased by precipitation reduction, while N concentration of foliage and litterfall significantly decreased. The combined effects of N addition and precipitation reduction significantly increased the δ13C and δ15N values of foliage as well as the δ15N values of fine roots and δ13C values of litterfall. Furthermore, foliar δ15N values were significantly correlated with foliage δ13C values, surface soil δ15N values, surface soil C concentration, and N concentrations. Nitrogen concentrations and δ13C values of foliage were significantly correlated with δ15N values and N concentrations of fine roots.ConclusionsThis indicates that plants increasingly take up the heavier 15N under N addition and the heavier 13C and 15N under precipitation reduction, suggesting that N addition and precipitation reduction may lead to more open forest ecosystem C and N cycling and affect plant nutrient acquisition strategies.

The geophagous earthworm Metaphire guillelmi effects on rhizosphere microbial community structure and functioning vary with plant species

The quantity and quality of plant-derived resources are the primary factors regulating soil microbial communities, however, the top-down control of soil fauna on the soil food web is still underexplored. To integrate bottom-up and top-down forces in mediating soil microbial communities, we evaluated six plant species rhizosphere microbial community structure (indicated by multiple PLFA biomarkers) and functioning (indicated by four different enzyme activities) in the presence and absence of seven adult Metaphire guillelmi earthworms. Six plant species with two legume species (Trifolium repens and Medicago sativa), two grass species (Arundo donax and Lolium perenne) and two grain crops (Triticum aestivum and Zea mays) were used varying with resource demand and nutrient acquisition strategies. We found earthworms led to increasing in similarity of rhizosphere microbial community structure across all studied plant species. For example, the variability of the fungi: bacteria and gram-positive: gram-negative ratios across six plant species was reduced in the presence of earthworms. Furthermore, earthworms generally supported enzyme production in acquiring carbon over nitrogen and phosphorus, and enhanced immobilization sink for N in microbial biomass, suggesting earthworms are more beneficial for microbes in acquiring energy as plant roots-produced enzyme mostly targeted on nutrients. In conclusion, our results revealed a context-dependent earthworm effects on microbial community structure and a general pattern of earthworms in shifting enzyme production across different plant species.

Correction to: Nutrient acquisition strategies in agroforestry systems

The following article is part of the Special Issue “Agroforestry: a belowground perspective” Guest Edited by Remi Cardinael, Zhun Mao, Claire Chenu, Philippe Hinsinger and was inadvertently published in a different issue