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1. Nitrogen is the major nutrient limiting plant growth in terrestrial ecosystems, and the transformation of inert nitrogen to forms that can be assimilated by plants is mediated by soil micro-organisms. 2 The last decade has witnessed many significant advances in our understanding of plant-microbe interactions with evidence that plants have evolved multiple strategies to cope with nitrogen limitation by shaping and recruiting nitrogen-cycling microbial communities. However, most studies have typically focused on the impact of plants on only one, or relatively few, processes within the nitrogen cycle. 3 This review synthesizes recent advances in our understanding of the various routes by which plants influence the availability of nitrogen via an array of interactions with different guilds of nitrogen-cycling micro-organisms. We also propose a plant trait-based framework for linking plant nitrogen acquisition strategies to the activities of nitrogen-cycling microbial guilds. In doing so, we provide a more comprehensive picture of the ecological relationships between plants and nitrogen-cycling micro-organisms in terrestrial ecosystems. 4 Finally, we identify previously overlooked processes within the nitrogen cycle that could be targeted in future research and be of interest for plant health or for improving plant nitrogen acquisition, while minimizing nitrogen inputs and losses in sustainable agricultural systems.

Boreal forest soils store a major proportion of the global terrestrial carbon (C) and below‐ground inputs contribute as much as above‐ground plant litter to the total C stored in the soil. A better understanding of the dynamics and drivers of root‐associated fungal communities is essential to predict long‐term soil C storage and climate feedbacks in northern ecosystems. We used 454‐pyrosequencing to identify fungal communities across fine‐scaled soil profiles in a 5000 yr fire‐driven boreal forest chronosequence, with the aim of pinpointing shifts in fungal community composition that may underlie variation in below‐ground C sequestration. In early successional‐stage forests, higher abundance of cord‐forming ectomycorrhizal fungi (such as Cortinarius and Suillus species) was linked to rapid turnover of mycelial biomass and necromass, efficient nitrogen (N) mobilization and low C sequestration. In late successional‐stage forests, cord formers declined, while ericoid mycorrhizal ascomycetes continued to dominate, potentially facilitating long‐term humus build‐up through production of melanized hyphae that resist decomposition. Our results suggest that cord‐forming ectomycorrhizal fungi and ericoid mycorrhizal fungi play opposing roles in below‐ground C storage. We postulate that, by affecting turnover and decomposition of fungal tissues, mycorrhizal fungal identity and growth form are critical determinants of C and N sequestration in boreal forests.

Symbiotic ectomycorrhizal fungi have received increasing attention as regulators of below-ground organic matter storage. They are proposed to promote organic matter accumulation by suppressing saprotrophs, but have also been suggested to play an active role in decomposition themselves. Here we show that exclusion of tree roots and associated ectomycorrhizal fungi in a boreal forest increased decomposition of surface litter by 11% by alleviating nitrogen limitation of saprotrophs–a “Gadgil effect”. At the same time, root exclusion decreased Mn-peroxidase activity in the deeper mor layer by 91%. Our results show that ectomycorrhizal fungi may hamper short-term litter decomposition, but also support a crucial role of ectomycorrhizal fungi in driving long-term organic matter oxidation. These observations stress the importance of ectomycorrhizal fungi in regulation of below-ground organic matter accumulation. By different mechanisms they may either hamper or stimulate decomposition, depending upon stage of decomposition and location in the soil profile.

Different symbiotic mycorrhizal associations between plants and fungi occur, almost ubiquitously, in a wide range of terrestrial ecosystems. Historically, these have mainly been considered within the rather narrow perspective of their effects on the uptake of dissolved mineral nutrients by individual plants. More recent research has placed emphasis on a wider, multifunctional perspective, including the effects of mycorrhizal symbiosis on plant and microbial communities, and on ecosystem processes. This includes mobilization of N and P from organic polymers, release of nutrients from mineral particles or rock surfaces via weathering, effects on carbon cycling, interactions with myco-heterotrophic plants, mediation of plant responses to stress factors such as drought, soil acidification, toxic metals, and plant pathogens, as well as a range of possible interactions with groups of other soil micro-organisms. Mycorrhizal fungi connect their plant hosts to the heterogeneously distributed nutrients required for their growth, enabling the flow of energy-rich compounds required for nutrient mobilization whilst simultaneously providing conduits for the translocation of mobilized products back to their hosts. In addition to increasing the nutrient absorptive surface area of their host plant root systems, the extraradical mycelium of mycorrhizal fungi provides a direct pathway for translocation of photosynthetically derived carbon to microsites in the soil and a large surface area for interaction with other micro-organisms. The detailed functioning and regulation of these mycorrhizosphere processes is still poorly understood but recent progress is reviewed and potential benefits of improved understanding of mycorrhizosphere interactions are discussed.

Plant nutrients can be recycled through microbial decomposition of organic matter but replacement of base cations and phosphorus, lost through harvesting of biomass/biofuels or leaching, requires de novo supply of fresh nutrients released through weathering of soil parent material (minerals and rocks). Weathering involves physical and chemical processes that are modified by biological activity of plants, microorganisms and animals. This article reviews recent progress made in understanding biological processes contributing to weathering. A perspective of increasing spatial scale is adopted, examining the consequences of biological activity for weathering from nanoscale interactions, through in vitro and in planta microcosm and mesocosm studies, to field experiments, and finally ecosystem and global level effects. The topics discussed include the physical alteration of minerals and mineral surfaces; the composition, amounts, chemical properties, and effects of plant and microbial secretions; and the role of carbon flow (including stabilisation and sequestration of C in organic and inorganic forms). Although the predominant focus is on the effects of fungi in forest ecosystems, the properties of biofilms, including bacterial interactions, are also discussed. The implications of these biological processes for modelling are discussed, and we attempt to identify some key questions and knowledge gaps, as well as experimental approaches and areas of research in which future studies are likely to yield useful results. A particular focus of this article is to improve the representation of the ways in which biological processes complement physical and chemical processes that mobilise mineral elements, making them available for plant uptake. This is necessary to produce better estimates of weathering that are required for sustainable management of forests in a post-fossil-fuel economy. While there are abundant examples of nanometre- and micrometre-scale physical interactions between microorganisms and different minerals, opinion appears to be divided with respect to the quantitative significance of these observations for overall weathering. Numerous in vitro experiments and microcosm studies involving plants and their associated microorganisms suggest that the allocation of plant-derived carbon, mineral dissolution and plant nutrient status are tightly coupled, but there is still disagreement about the extent to which these processes contribute to field-scale observations. Apart from providing dynamically responsive pathways for the allocation of plant-derived carbon to power dissolution of minerals, mycorrhizal mycelia provide conduits for the long-distance transportation of weathering products back to plants that are also quantitatively significant sinks for released nutrients. These mycelial pathways bridge heterogeneous substrates, reducing the influence of local variation in C:N ratios. The production of polysaccharide matrices by biofilms of interacting bacteria and/or fungi at interfaces with mineral surfaces and roots influences patterns of production of antibiotics and quorum sensing molecules, with concomitant effects on microbial community structure, and the qualitative and quantitative composition of mineral-solubilising compounds and weathering products. Patterns of carbon allocation and nutrient mobilisation from both organic and inorganic substrates have been studied at larger spatial and temporal scales, including both ecosystem and global levels, and there is a generally wider degree of acceptance of the “systemic” effects of microorganisms on patterns of nutrient mobilisation. Theories about the evolutionary development of weathering processes have been advanced but there is still a lack of information connecting processes at different spatial scales. Detailed studies of the liquid chemistry of local weathering sites at the micrometre scale, together with upscaling to soil-scale dissolution rates, are advocated, as well as new approaches involving stable isotopes.

Ectomycorrhizal (ECM) symbioses have evolved a minimum of 78 times independently from saprotrophic lineages, indicating the potential for functional overlap between ECM and saprotrophic fungi. ECM fungi have the capacity to decompose organic matter, and although there is increasing evidence that some saprotrophic fungi exhibit the capacity to enter into facultative biotrophic relationships with plant roots without causing disease symptoms, this subject is still not well studied. In order to determine the extent of biotrophic capacity in saprotrophic wood-decay fungi and which systems may be useful models, we investigated the colonization of conifer seedling roots in vitro using an array of 201 basidiomycete wood-decay fungi. Microtome sectioning, differential staining and fluorescence microscopy were used to visualize patterns of root colonization in microcosm systems containing Picea abies or Pinus sylvestris seedlings and each saprotrophic fungus. Thirty-four (16.9%) of the tested fungal species colonized the roots of at least one tree species. Two fungal species showed formation of a mantle and one showed Hartig net-like structures. These features suggest the possibility of an active functional symbiosis between fungus and plant. The data indicate that the capacity for facultative biotrophic relationships in free-living saprotrophic basidiomycetes may be greater than previously supposed.

The oxalate-carbonate pathway (OCP) involves degradation of soil oxalate to carbonate. To exploit and manage this natural mineralization of assimilated atmospheric CO 2 into stable carbonates, improved understanding of this complex biotransformation process is needed. A strain of oxalate-degrading bacteria, Azospirillum sp. OX-1, was isolated from soil, and its secondary products of calcium oxalate degradation were analyzed and characterized using SEM, XRD, TG/DTG-DTA and FTIR-spectroscopy. The molecular mechanism of calcium oxalate degradation was also analyzed using proteomics. The results showed, for the first time, that OX-1 could not only degrade calcium oxalate to calcium carbonate, but also that the process was accompanied by synthesis of methane. Proteomic analysis demonstrated that OX-1 has a dual enzyme system for calcium oxalate degradation, using formyl-CoA transferase (FRC) and thiamine pyrophosphate (ThDP)-dependent oxalyl-CoA decarboxylase (OXC) to form calcium carbonate. Up-regulated expression of enzymes related to methane synthesis was also detected during calcium oxalate degradation. Since methane is also a potent greenhouse gas, these new results suggest that the utility of exploiting the OCP to reduce atmospheric CO 2 must be re-evaluated and that further studies should be conducted to reveal how widespread the methane producing capacity of strain OX-1 is in other bacteria and soil environments.

In boreal forest soils, ectomycorrhizal fungi are fundamentally important for carbon (C) dynamics and nutrient cycling. Although their extraradical mycelium (ERM) is pivotal for processes such as soil organic matter build-up and nitrogen cycling, very little is known about its dynamics and regulation. In this study, we quantified ERM production and turnover, and examined how these two processes together regulated standing ERM biomass in seven sites forming a chronosequence of 12- to 100-yr-old managed Pinus sylvestris forests. This was done by determining ERM biomass, using ergosterol as a proxy, in sequentially harvested in-growth mesh bags and by applying mathematical models. Although ERM production declined with increasing forest age from 1.2 to 0.5 kg ha−1 d−1, the standing biomass increased from 50 to 112 kg ha−1. This was explained by a drastic decline in mycelial turnover from seven times to one time per year with increasing forest age, corresponding to mean residence times from 25 d up to 1 yr. Our results demonstrate that ERM turnover is the main factor regulating biomass across differently aged forest stands. Explicit inclusion of ERM parameters in forest ecosystem C models may significantly improve their capacity to predict responses of mycorrhiza-mediated processes to management and environmental changes.

Boreal forests are characterized by spatially heterogeneous soils with low N availability. The decomposition of coniferous litter in these systems is primarily performed by basidiomycete fungi, which often form large mycelia with a well-developed capacity to reallocate resources spatially- an advantageous trait in heterogeneous environments. In axenic microcosm systems we tested whether fungi increase their biomass production by reallocating N between Pinus sylvestris (Scots pine) needles at different stages of decomposition. We estimated fungal biomass production by analysing the accumulation of the fungal cell wall compound chitin. Monospecific systems were compared with systems with interspecific interactions. We found that the fungi reallocated assimilated N and mycelial growth away from well-degraded litter towards fresh litter components. This redistribution was accompanied by reduced decomposition of older litter. Interconnection of substrates increased over-all fungal C use efficiency (i.e. the allocation of assimilated C to biomass rather than respiration), presumably by enabling fungal translocation of growth-limiting N to litter with higher C quality. Fungal connection between different substrates also restricted N-mineralization and production of dissolved organic N, suggesting that litter saprotrophs in boreal forest ecosystems primarily act to redistribute rather than release N. This spatial integration of different resource qualities was hindered by interspecific interactions, in which litters of contrasting quality were colonised by two different basidiomycete species. The experiments provide a detailed picture of how resource reallocation in two decomposer fungi leads to a more efficient utilisation of spatially separated resources under N-limitation. From an ecosystem point of view, such economic fungal behaviour could potentially contribute to organic matter accumulation in the litter layers of boreal forests.