No Significant Contribution of Arbuscular Mycorrhizal Fungi to Transfer of Radiocesium from Soil to Plants

The diffuse pollution by fission and activation products following nuclear accidents and weapons testing is of major public concern. Among the nuclides that pose a serious risk if they enter the human food chain are the cesium isotopes ¹³⁷Cs and ¹³⁴Cs (with half-lives of 30 and 2 years, respectively). The biogeochemical cycling of these isotopes in forest ecosystems is strongly affected by their preferential absorption in a range of ectomycorrhiza-forming basidiomycetes. An even more widely distributed group of symbiotic fungi are the arbuscular mycorrhizal fungi, which colonize most herbaceous plants, including many agricultural crops. These fungi are known to be more efficient than ectomycorrhizas in transporting mineral elements from soil to plants. Their role in the biogeochemical cycling of Cs is poorly known, in spite of the consequences that fungal Cs transport may have for transfer of Cs into the human food chain. This report presents the first data on transport of Cs by these fungi by use of radiotracers and compartmented growth systems where uptake by roots and mycorrhizal hyphae is distinguished. Independent experiments in three laboratories that used different combinations of fungi and host plants all demonstrated that these fungi do not contribute significantly to plant uptake of Cs. The implications of these findings for the bioavailability of radiocesium in different terrestrial ecosystems are discussed.     

菌根真菌在生态系统中的作用

 菌根是一种植物营养根与土壤真菌形成的共生体,在自然界中分布广泛。本文着重从以下几个方面介绍相关的研究进展：1) 菌根真菌作为生态系统的重要组成部分,具有不可忽视的生物量,并成为连接绿色植物和食真菌者食物链的重要一环;2) 菌根真菌通过参与凋落物的酶降解过程影响有机物的循环,通过促进生物固氮、加速土壤磷的风化、提高土壤溶液离子的有效性以及直接吸收等过程影响氮、磷、钾、钙、镁等元素的无机循环;3) 菌根真菌与土壤微生物间存在有益的或拮抗的相互作用,并可以直接或间接地影响根际生物区系的组成和数量;菌根真菌通过对宿主植物的有益作用而影响植物的种间竞争,通过菌根网络而形成的种团可以在同种或不同种植物间实现资源的重新分配和共享;由于对种间关系的作用和对食物链的影响,菌根真菌对群落的物种构成和多样性的维持具有重要的作用;菌根真菌是群落演替过程的指示者,也是这一过程的参与者和推动者,并且菌根真菌的存在也有利于提高土壤团聚体的稳定性及促进灰壤的形成;4) 菌根真菌的种类和数量可以指示生态系统中自然的或人类活动引起的变化,并可以在生态系统的保护、恢复或重建过程中发挥重要作用。文章的最后还介绍了最新的研究热点和发展趋势。     

Extraradical mycelium of the arbuscular mycorrhizal fungus Glomus lamellosum can take up,accumulate and translocate radiocaesium under root-organ culture conditions

Radiocaesium enters the food chain when plants absorb it from soil, in a process that is strongly dependent on soil properties and plant and microbial species. Among the microbial species, arbuscular mycorrhizal (AM) fungi are obligate symbionts that colonize the root cortex of many plants and develop an extraradical mycelial (ERM) network that ramifies in the soil. Despite the well-known involvement of this ERM network in mineral nutrition and uptake of some heavy metals, only limited data are available on its role in radiocaesium transport in plants. We used root-organ culture to demonstrate that the ERM of the AM fungus Glomus lamellosum can take up, possibly accumulate and unambiguously translocate radiocaesium from a 137Cs-labelled synthetic root-free compartment to a root compartment and within the roots. The accumulation of 137Cs by hyphae in the root-free compartment may be explained by sequestration in the hyphae or by a bottleneck effect resulting from a limited number of hyphae crossing the partition between the two compartments. Uptake and translocation resulted from the incorporation of 137Cs into the fungal hyphae, as no 137Cs was detected in mycorrhizal roots treated with formaldehyde. The importance of the translocation process was indicated by the correlation between 137Cs measured in the roots and the total hyphal length connecting the roots with the labelled compartment. 137Cs may be translocated via a tubular vacuolar system or by cytoplasmic streaming per se.     

菌根真菌与植物共生营养交换机制研究进展

菌根是陆地生态系统普遍存在的、由土壤中的菌根真菌侵染宿主植物根系形成的联合共生体.菌根的建立是以共生体双方的营养交换为基础的:菌根真菌从土壤中吸收氮、磷等营养物质并转运给宿主植物,供其生长;作为交换,植物则以脂质或糖的形式向菌根真菌提供其生长所必需的碳水化合物.近年来,菌根真菌与宿主植物间的营养交换机制一直是研究的热点,国内外对菌根真菌介导的植物营养物质吸收和转运机制的研究也取得了巨大进展.本文综述了丛枝和外生两种菌根真菌与宿主植物间营养交换的最新研究进展,尤其是碳、氮、磷等几种重要营养物质的吸收与双向转运机制,以及营养交换在菌根形成中的潜在调控作用,并对目前存在的关键问题和未来研究方向进行了分析和展望,这对菌根模型的建立及菌根效益的优化具有重要意义.     

Transport of radiocaesium by arbuscular mycorrhizal fungi to Medicago truncatula under in vitro conditions

The capacity of arbuscular mycorrhizal (AM) fungi to take up and translocate radiocaesium (Cs) to their host has been shown using the root-organ culture (ROC) system. However, the absence of photosynthetic tissues, lack of a normal root hormonal balance and incomplete source-sink relationships may bias the bidirectional transfer of elements at the symbiotic interface and complicate transport studies. Accordingly, we developed a novel culture system [i.e. the Arbuscular Mycorrhizal-Plant (AM-P) in vitro culture system], where AM fungi and an autotrophic host plant develop under strict in vitro conditions. With this system, we unambiguously demonstrated the capacity of AM fungi to transport Cs. The extraradical fungal hyphae took up 21.0% of the initial supply of 134Cs. Translocation to the plant represented 83.6% of the 134Cs taken up. Distribution of 134Cs in the host plant was 89.8% in the mycorrhizal roots and 10.2% in the shoot. These results confirm that AM fungi can take up, translocate and accumulate Cs. They further demonstrate unambiguously and for the first time that Cs can be transferred from AM fungi to host tissues. These results suggest a potential involvement of AM fungi in Cs biogeochemical cycle and in plant Cs accumulation.     

How can increased use of biological N2 fixation in agriculture benefit the environment?

Caesium (Cs) is an alkali metal with chemical properties similar to potassium (K). It has no known role in plant nutrition and it is not toxic to plants at the micromolar concentrations occurring naturally in soil solutions. However, two radioisotopes of Cs (¹³⁴Cs and ¹³⁷Cs) are of environmental concern due to their relatively long half-lives, emissions of and radiation during decay, and rapid incorporation into biological systems. There is considerable interest in remediating sites contaminated by these isotopes using phytoextraction and, since the produce from radiocaesium-contaminated areas may enter the food chain, the introduction of `safe' crops that do not accumulate Cs. This article reviews the molecular mechanisms of Cs uptake by plants, and provides a perspective on strategies to develop: (1) plants that extract Cs efficiently from soils (for the phytoremediation of land), or (2) `safe' crops that minimise the entry of radiocaesium directly into the human food chain.     

The role of fungi in biogenic weathering in boreal forest soils

In this article we discuss the possible significance of biological processes, and of fungi in particular, in weathering of minerals. We consider biological activity to be a significant driver of mineral weathering in forest ecosystems. In these environments fungi play key roles in organic matter decomposition, uptake, transfer and cycling of organic and inorganic nutrients, biogenic mineral formation, as well as transformation and accumulation of metals. The ability of lichens, mutualistic symbioses between fungi and photobionts such as algae or cyanobacteria, to weather minerals is well documented. The role of mycorrhizal fungi forming symbioses with forest trees is less well understood, but the mineral horizons of boreal forests are intensively colonised by mycorrhizal mycelia which transfer protons and organic metabolites derived from plant photosynthates to mineral surfaces, resulting in mineral dissolution and mobilisation and redistribution of anionic nutrients and metal cations. The mycorrhizal mycelia, in turn provide efficient systems for the uptake and direct transport of mobilised essential nutrients to their host plants which are large sinks. Since almost all (99.99 %) non-suberised lateral plant roots involved in nutrient uptake are covered by ectomycorrhizal fungi, most of this exchange of metabolites must take place through the plant–fungus interface. This idea is still consistent with a linear relationship between soil mineral surface area and weathering rate since the mycelia that emanate from the tree roots will have a larger area of contact with minerals if the mineral surface area is higher. Although empirical models based on bulk soil solution chemistry may fit field data, we argue that biological processes make an important contribution to mineral weathering and that a more detailed mechanistic understanding of these must be developed in order to predict responses to environmental changes and anthropogenic impact.     

Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses

Forest ecosystems with low soil nitrogen (N) availability are characterized by direct competition for this growth-limiting resource between several players, i.e. various components of vegetation, such as old-growth trees, natural regeneration and understorey species, mycorrhizal fungi, free-living fungi and bacteria. With the increase in frequency and intensity of extreme climate events predicted in current climate change scenarios, also competition for N between plants and/or soil microorganisms will be affected. In this review, we summarize the present understanding of ecosystem N cycling in N-limited forests and its interaction with extreme climate events, such as heat, drought and flooding. More specifically, the impacts of environmental stresses on microbial release and consumption of bioavailable N, N uptake and competition between plants, as well as plant and microbial uptake are presented. Furthermore, the consequences of drying–wetting cycles on N cycling are discussed. Additionally, we highlight the current methodological difficulties that limit present understanding of N cycling in forest ecosystems and the need for interdisciplinary studies.     

菌根真菌影响森林生态系统碳循环研究进展

森林生态系统在全球碳(C)储量中占据极为重要的地位。菌根真菌广泛存在于森林生态系统中,在森林生态系统C循环过程中发挥重要的作用。阐述了不同菌根类型真菌在森林生态系统C循环过程中的功能,对比了温带/北方森林与热带/亚热带森林中菌根真菌介导的C循环研究方面新近取得的研究结果。发现温带和北方森林的外生菌根(EcM)植物对地上生物量C的贡献相对较小,然而是地下C储量的主要贡献者;以丛枝菌根(AM)共生为主的热带/亚热带森林地表生物量占比较高,表明AM植被对热带/亚热带森林地上生物量C的贡献相对较大。我们还就全球变化背景下,菌根真菌及其介导的森林生态系统C汇功能,以及不同菌根类型树种影响C循环的机制等进行了总结。菌根真菌通过影响凋落物分解、土壤有机质形成及地下根系生物量,进而影响整个森林生态系统的C循环功能。菌根介导的森林C循环过程很大程度上取决于(优势)树木的菌根类型和森林土壤中菌根真菌的群落结构。最后指出了当前研究存在的主要问题以及未来研究展望。本文旨在明确菌根真菌在森林生态系统C循环转化过程中的重要生态功能,有助于准确地评估森林生态系统C汇现状,为应对全球变化等提供重要的依据。     

13C and 15N in microarthropods reveal little response of Douglas-fir ecosystems to climate change

Understanding ecosystem carbon (C) and nitrogen (N) cycling under global change requires experiments maintaining natural interactions among soil structure, soil communities, nutrient availability, and plant growth. In model Douglas-fir ecosystems maintained for five growing seasons, elevated temperature and carbon dioxide (CO₂) increased photosynthesis and increased C storage belowground but not aboveground. We hypothesized that interactions between N cycling and C fluxes through two main groups of microbes, mycorrhizal fungi (symbiotic with plants) and saprotrophic fungi (free-living), mediated ecosystem C storage. To quantify proportions of mycorrhizal and saprotrophic fungi, we measured stable isotopes in fungivorous microarthropods that efficiently censused the fungal community. Fungivorous microarthropods consumed on average 35% mycorrhizal fungi and 65% saprotrophic fungi. Elevated temperature decreased C flux through mycorrhizal fungi by 7%, whereas elevated CO₂ increased it by 4%. The dietary proportion of mycorrhizal fungi correlated across treatments with total plant biomass (n= 4, r²= 0.96, P= 0.021), but not with root biomass. This suggests that belowground allocation increased with increasing plant biomass, but that mycorrhizal fungi were stronger sinks for recent photosynthate than roots. Low N content of needles (0.8–1.1%) and A horizon soil (0.11%) coupled with high C : N ratios of A horizon soil (25–26) and litter (36–48) indicated severe N limitation. Elevated temperature treatments increased the saprotrophic decomposition of litter and lowered litter C : N ratios. Because of low N availability of this litter, its decomposition presumably increased N immobilization belowground, thereby restricting soil N availability for both mycorrhizal fungi and plant growth. Although increased photosynthesis with elevated CO₂ increased allocation of C to ectomycorrhizal fungi, it did not benefit plant N status. Most N for plants and soil storage was derived from litter decomposition. N sequestration by mycorrhizal fungi and limited N release during litter decomposition by saprotrophic fungi restricted N supply to plants, thereby constraining plant growth response to the different treatments.     

Interpretation of nitrogen isotope signatures using the NIFTE model

Nitrogen cycling in forest soils has been intensively studied for many years because nitrogen is often the limiting nutrient for forest growth. Complex interactions between soil, microbes, and plants and the consequent inability to correlate δ¹⁵N changes with biologic processes have limited the use of natural abundances of nitrogen isotopes to study nitrogen (N) dynamics. During an investigation of N dynamics along the 250-year-old successional sequence in Glacier Bay, Alaska, United States, we observed several puzzling isotopic patterns, including a consistent decline in δ¹⁵N of the late successional dominant Picea at older sites, a lack of agreement between mineral N δ¹⁵N and foliar δ¹⁵N, and high isotopic signatures for mycorrhizal fungi. In order to understand the mechanisms creating these patterns, we developed a model of N dynamics and N isotopes (Nitrogen Isotope Fluxes in Terrestrial Ecosystems, NIFTE), which simulated the major transformations of the N cycle and predicted isotopic signatures of different plant species and soil pools. Comparisons with field data from five sites along the successional sequence indicated that NIFTE can duplicate observed patterns in δ¹⁵N of soil, foliage, and mineral N over time. Different scenarios that could account for the observed isotopic patterns were tested in model simulations. Possible mechanisms included increased isotopic fractionation on mineralization, fractionation during the transfer of nitrogen from mycorrhizal fungi to plants, variable fractionation on uptake by mycorrhizal fungi compared to plants, no fractionation on mycorrhizal transfer, and elimination of mycorrhizal fungi as a pool in the model. The model results suggest that fractionation during mineralization must be small (˜2‰), and that no fractionation occurs during plant or mycorrhizal uptake. A net fractionation during mycorrhizal transfer of nitrogen to vegetation provided the best fit to isotopic data on mineral N, plants, soils, and mycorrhizal fungi. The model and field results indicate that the importance of mycorrhizal fungi to N uptake is probably less under conditions of high N availability. Use of this model should encourage a more rigorous assessment of isotopic signatures in ecosystem studies and provide insights into the biologic transformations which affect those signatures. This should lead to an enhanced understanding of some of the fundamental controls on nitrogen dynamics. Received: 1 July 1998 / Accepted: 23 December 1998     

Multi-functionality and biodiversity in arbuscular mycorrhizas

Plant roots in natural ecosystems are typically colonized by a wide range of fungi. Some of these are pathogenic, others appear to be opportunistic and have no apparent impact, while mycorrhizal fungi are generally regarded as mutualistic. Of the various types of mycorrhizal fungi, the arbuscular mycorrhizal (AM) association is by far the most abundant and widespread. While the most widely accepted model of AM function depends upon plants benefiting from the facilitation of phosphorus uptake, recent data from field-based studies in temperate ecosystems indicate that only plant species with poorly branched root systems benefit from AM fungi in this way: species with highly branched root systems may benefit in other ways, such as by being protected against root pathogenic fungi. These two responses apparently represent extremes along a continuum of AM benefit determined by root system architecture.     

Differential C isotope discrimination by fungi during decomposition of C(3)- and C(4)-derived sucrose

Stable isotope analysis is a major tool used in ecosystem studies to establish pathways and rates of C exchange between various ecosystem components. Little is known about isotopic effects of many such components, especially microbes. Here we report on the discovery of an unexpected pattern of C isotopic discrimination by basidiomycete fungi with far-reaching consequences for our understanding of isotopic processing in ecosystems where these microbes mediate material transfers across trophic levels. We measured fractionation effects on three ecologically relevant basidiomycete species under controlled laboratory conditions. Sucrose derived from C(3) and C(4) plants is fractionated differentially by these microbes in a taxon-specific manner. The differentiation between mycorrhizal and saprotrophic fungi observed in the field by others is not explained by intrinsic discrimination patterns. Fractionation occurs during sugar uptake and is sensitive to the nonrandom distribution of stable isotopes in the sucrose molecule. The balance between respiratory physiology and fermentative physiology modulates the degree of fractionation. These discoveries disprove the assumption that fungal C processing does not significantly alter the distribution of stable C isotopes and provide the basis for a reevaluation of ecosystem models based on isotopic evidence that involve C transfer across microbial interfaces. We provide a mechanism to account for the observed differential discrimination effects.     

Contribution of the arbuscular mycorrhizal symbiosis to heavy metal phytoremediation

High concentrations of heavy metals (HM) in the soil have detrimental effects on ecosystems and are a risk to human health as they can enter the food chain via agricultural products or contaminated drinking water. Phytoremediation, a sustainable and inexpensive technology based on the removal of pollutants from the environment by plants, is becoming an increasingly important objective in plant research. However, as phytoremediation is a slow process, improvement of efficiency and thus increased stabilization or removal of HMs from soils is an important goal. Arbuscular mycorrhizal (AM) fungi provide an attractive system to advance plant-based environmental clean-up. During symbiotic interaction the hyphal network functionally extends the root system of their hosts. Thus, plants in symbiosis with AM fungi have the potential to take up HM from an enlarged soil volume. In this review, we summarize current knowledge about the contribution of the AM symbiosis to phytoremediation of heavy metals.     

Differential C Isotope Discrimination by Fungi during Decomposition of C3- and C4-Derived Sucrose

Stable isotope analysis is a major tool used in ecosystem studies to establish pathways and rates of C exchange between various ecosystem components. Little is known about isotopic effects of many such components, especially microbes. Here we report on the discovery of an unexpected pattern of C isotopic discrimination by basidiomycete fungi with far-reaching consequences for our understanding of isotopic processing in ecosystems where these microbes mediate material transfers across trophic levels. We measured fractionation effects on three ecologically relevant basidiomycete species under controlled laboratory conditions. Sucrose derived from C₃ and C₄ plants is fractionated differentially by these microbes in a taxon-specific manner. The differentiation between mycorrhizal and saprotrophic fungi observed in the field by others is not explained by intrinsic discrimination patterns. Fractionation occurs during sugar uptake and is sensitive to the nonrandom distribution of stable isotopes in the sucrose molecule. The balance between respiratory physiology and fermentative physiology modulates the degree of fractionation. These discoveries disprove the assumption that fungal C processing does not significantly alter the distribution of stable C isotopes and provide the basis for a reevaluation of ecosystem models based on isotopic evidence that involve C transfer across microbial interfaces. We provide a mechanism to account for the observed differential discrimination effects.     

Defining nutritional constraints on carbon cycling in boreal forests – towards a less `phytocentric' perspective

Growing interest in possible global climate change has underlined the need for better information concerning the way in which carbon partitioning between ecosystem components is influenced by constraints on nutrient availability. Micro-organisms play a fundamental role in the cycling of carbon and nutrients in all ecosystems but the role of fungi in particular is pivotal in boreal forest ecosystems. Traditional models of nutrient cycling are based on methods and concepts developed in agricultural systems where microorganisms are considered primarily as nutrient processors providing plants with inorganic nutrients. The filamentous nature of fungi, their ability to translocate carbon and nutrients between different substrates and the capacity of ectomycorrhizal fungi to utilise organic nutrients have all been largely ignored. In this article, a new model is suggested which emphasises competition for organic nutrients between decomposer organisms and plants, with the plants depending on their associated mycorrhizal fungi for nutrient acquisition. Antagonistic interactions involving nutrient transfer between decomposer and mycorrhizal fungi are proposed as important pathways in nutrient cycling. Due to the nutrient conservative features of decomposer fungi, inorganic nutrients are considered less important for plant nutrition. The implications of the new nutrient cycling model on the carbon balance of boreal forests are discussed.     

菌根真菌对土壤呼吸以及凋落物分解的影响

土壤呼吸是植物固定的碳由陆地生态系统进入大气的主要途径之一; 凋落物分解是养分循环的重要环节。陆地植物的90%以上可同菌根真菌形成共生关系, 菌根真菌对于植物获取环境中的养分具有重要的作用。然而, 其对土壤呼吸和凋落物分解的影响却经常在生态系统对环境变化的响应研究中被忽视。本文系统地综述了国内外相关研究进展, 对菌根真菌如何影响土壤呼吸和凋落物分解这两个过程及这种影响如何受到环境变化的制约做了全面的分析, 并对以往研究中存在的问题以及未来的研究方向提出了展望。     

Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest

Our understanding of how saprotrophic and mycorrhizal fungi interact to re-circulate carbon and nutrients from plant litter and soil organic matter is limited by poor understanding of their spatiotemporal dynamics. In order to investigate how different functional groups of fungi contribute to carbon and nitrogen cycling at different stages of decomposition, we studied changes in fungal community composition along vertical profiles through a Pinus sylvestris forest soil. We combined molecular identification methods with 14C dating of the organic matter, analyses of carbon:nitrogen (C:N) ratios and 15N natural abundance measurements. Saprotrophic fungi were primarily confined to relatively recently (< 4 yr) shed litter components on the surface of the forest floor, where organic carbon was mineralized while nitrogen was retained. Mycorrhizal fungi dominated in the underlying, more decomposed litter and humus, where they apparently mobilized N and made it available to their host plants. Our observations show that the degrading and nutrient-mobilizing components of the fungal community are spatially separated. This has important implications for biogeochemical studies of boreal forest ecosystems.     

Are there edge effects on forest fungi and if so do they matter?

Fungi are vital within forest ecosystems through their mycorrhizal relationships with trees, and as the main agents of wood decomposition and thus carbon and nutrient cycling. Globally, forests are becoming increasingly fragmented, creating forest patches that are isolated, reduced in area, and exposed at edges. Edges are often ecologically distinct from the forest interior due to their exposure to the matrix habitat. This exposure can result in altered microclimatic conditions and flows of biotic and abiotic materials such as spores or inorganic nitrogen, respectively.Although fungi are known to be affected by microclimate and nitrogen deposition, knowledge of forest edge effects on fungi is extremely limited; however, a consideration of the factors known to regulate fungal activity in combination with known biotic and abiotic edge effects implies that forest edges are likely to strongly influence fungi. These include responses of fungi to the altered microclimate and nitrogen levels at forest edges, at both the individual and community level; interactions with plants and animals that have been influenced by edges; above–belowground feedback between mycorrhizal fungi and host trees. The small body of existing research focuses on fruit body presence and distribution; fungal biomass and community composition in soil have been touched upon. Positive, negative and neutral edge responses have been found, the majority of studies finding a significant effect on some of the parameters measured. Generally, abundance of fruit bodies and biomass in the soil is lower at the forest edge.Understanding how fungi respond to edges is essential to a more complete knowledge of carbon and nitrogen cycling in forest edges, influence of mycorrhizal species on vegetation, and conservation of rare fungi. As edges become increasingly dominant landscape features it is vital to investigate processes within them, to understand ecosystem function at a landscape scale.     

城市菌根真菌多样性、变化机制及功能应用

菌根真菌能够与大多数陆生植物的根系形成菌根共生体,具有改善宿主植物矿质营养、增强抗逆性、改良土壤结构等重要生态功能。城市化过程中气候、土壤、植被、土地利用等因素的改变,对菌根真菌的多样性产生了直接或间接的影响。目前城市菌根真菌的研究多侧重对其空间分布及群落组成的简单描述,缺乏针对城市典型生态现象及生态问题系统性的探讨。分别从城市菌根真菌的多样性变化、影响机制及功能应用等3方面进行了综述,全面揭示城市菌根真菌的研究现状及研究的复杂性,发现当前研究存在多样性评估简单化、研究层次单一化、内在机制现象化及功能应用停滞化等问题,认为今后应建立更为系统、综合、标准的研究体系以深刻而准确地认识与理解城市化对菌根真菌多样性的影响,为城市微生物资源的保存及绿地系统维持提供理论依据。