Roger D. Finlay

Carbon flow in the rhizosphere: carbon trading at the soil-root interface

The loss of organic and inorganic carbon from roots into soil underpins nearly all the major changes that occur in the rhizosphere. In this review we explore the mechanistic basis of organic carbon and nitrogen flow in the rhizosphere. It is clear that C and N flow in the rhizosphere is extremely complex, being highly plant and environment dependent and varying both spatially and temporally along the root. Consequently, the amount and type of rhizodeposits (e.g. exudates, border cells, mucilage) remains highly context specific. This has severely limited our capacity to quantify and model the amount of rhizodeposition in ecosystem processes such as C sequestration and nutrient acquisition. It is now evident that C and N flow at the soil–root interface is bidirectional with C and N being lost from roots and taken up from the soil simultaneously. Here we present four alternative hypotheses to explain why high and low molecular weight organic compounds are actively cycled in the rhizosphere. These include: (1) indirect, fortuitous root exudate recapture as part of the root’s C and N distribution network, (2) direct re-uptake to enhance the plant’s C efficiency and to reduce rhizosphere microbial growth and pathogen attack, (3) direct uptake to recapture organic nutrients released from soil organic matter, and (4) for inter-root and root–microbial signal exchange. Due to severe flaws in the interpretation of commonly used isotopic labelling techniques, there is still great uncertainty surrounding the importance of these individual fluxes in the rhizosphere. Due to the importance of rhizodeposition in regulating ecosystem functioning, it is critical that future research focuses on resolving the quantitative importance of the different C and N fluxes operating in the rhizosphere and the ways in which these vary spatially and temporally.

Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest

Forest Fungi Boreal forest is one of the worlds major biomes, dominating the subarctic northern latitudes of Europe, Asia, and America. The soils of boreal forest function as a net sink in the global carbon cycle and, hitherto, it has been thought that organic matter in this sink primarily accumulates in the form of plant remains. Clemmensen et al. (p. 1615; see the Perspective by Treseder and Holden) now show that most of the stored carbon in boreal forested islands in Sweden is in fact derived from mycorrhizal mycelium rather than from plant litter. Biochemical and sequencing studies show that carbon sequestration is regulated by functional and phylogenetic shifts in the mycorrhizal fungal community. The results will need to be explicitly considered in models of the role of the boreal forest in the global carbon cycle. Reservoirs of carbon in boreal forest soils are revisited in an island chronosequence, using modeling and molecular approaches. [Also see Perspective by Treseder and Holden] Boreal forest soils function as a terrestrial net sink in the global carbon cycle. The prevailing dogma has focused on aboveground plant litter as a principal source of soil organic matter. Using 14C bomb-carbon modeling, we show that 50 to 70% of stored carbon in a chronosequence of boreal forested islands derives from roots and root-associated microorganisms. Fungal biomarkers indicate impaired degradation and preservation of fungal residues in late successional forests. Furthermore, 454 pyrosequencing of molecular barcodes, in conjunction with stable isotope analyses, highlights root-associated fungi as important regulators of ecosystem carbon dynamics. Our results suggest an alternative mechanism for the accumulation of organic matter in boreal forests during succession in the long-term absence of disturbance.

Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture

In sustainable, low-input cropping systems the natural roles of microorganisms in maintaining soil fertility and biocontrol of plant pathogens may be more important than in conventional agriculture where their significance has been marginalised by high inputs of agrochemicals. Better understanding of the interactions between arbuscular mycorrhizal fungi and other microorganisms is necessary for the development of sustainable management of soil fertility and crop production. Many studies of the influence of mycorrhizal colonisation on associated bacterial communities have been conducted, however, the mechanisms of interaction are still poorly understood. Novel approaches including PCR-based methods, stable isotope profiling, and molecular markers have begun to shed light on the activity, identity and spatiotemporal location of bacteria in the mycorrhizosphere. This paper reviews current knowledge concerning the interactions between arbuscular mycorrhizal fungi and other microorganisms, particularly bacteria, and discusses the implications these interactions may have in sustainable agriculture.

Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals

Plant nutrients, with the exception of nitrogen, are ultimately derived from weathering of primary minerals. Traditional theories about the role of ectomycorrhizal fungi in plant nutrition have emphasized quantitative effects on uptake and transport of dissolved nutrients. Qualitative effects of the symbiosis on the ability of plants to access organic nitrogen and phosphorus sources have also become increasingly apparent. Recent research suggests that ectomycorrhizal fungi mobilize other essential plant nutrients directly from minerals through excretion of organic acids. This enables ectomycorrhizal plants to utilize essential nutrients from insoluble mineral sources and affects nutrient cycling in forest systems.

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.

Carbon sequestration is related to mycorrhizal fungal community shifts during long‐term succession in boreal forests

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.

Advances in understanding the podzolization process resulting from a multidisciplinary study of three coniferous forest soils in the Nordic Countries

Advances in understanding the podzolisation process resulting from a multidisciplinary study at three coniferous forest soils in the Nordic countries

Exudation-reabsorption in a mycorrhizal fungus, the dynamic interface for interaction with soil and soil microorganisms

Abstract The mycelium of Suillus bovinus slowly absorbed [U-14C]glucose and other tracers from droplets placed on the cords, translocated them to the peripheral hyphae and exuded them into fluid drops on the hyphal tips. The exudate was characterized by 1H NMR spectroscopy and by sugar and amino acid analysis. The exuded compounds were mainly carbohydrates and peptides. Acetic acid and oxalic acid were also present in the exudate along with a number of unidentified compounds. Released ions (K, Na, Cl, P, Mg and Ca) were identified by X-ray microanalysis. The mycelium was shown to reabsorb up to 65% of the exuded 14C compounds in 2 days. Glucose, mannitol, glutamic acid (pH 3.2), and Rb+ (as well as other mineral ions) were all readily absorbed by the mycelium, while oxalic acid at pH 4.2 and glutamic acid at pH 6.5 were not. Exudation of fluid droplets on the surface of the hydrophobic mycorrhizal fungus S. bovinus may represent an ecophysiologically important function of the extramatrical hyphae, which provides an interface for interaction with the immediate hyphal environment and its other microorganisms where the peripheral hyphae exchange their photosynthetically derived products for nutrients to be used later by the pine host. We hypothesize that actively absorbed carbohydrates from the root are translocated to the peripheral hyphae along a concentration gradient of sugars and polyols by means of active translocation and diffusion in cell elements and by acropetal water transport in the cord vessels.

Fungal communities in mycorrhizal roots of conifer seedlings in forest nurseries under different cultivation systems, assessed by morphotyping, direct sequencing and mycelial isolation

Fungi colonising root tips of Pinus sylvestris and Picea abies grown under four different seedling cultivation systems were assessed by morphotyping, direct sequencing and isolation methods. Roots were morphotyped using two approaches: (1) 10% of the whole root system from 30 seedlings of each species and (2) 20 randomly selected tips per plant from 300 seedlings of each species. The first approach yielded 15 morphotypes, the second yielded 27, including 18 new morphotypes. The overall community consisted of 33 morphotypes. The level of mycorrhizal colonisation of roots determined by each approach was about 50%. The cultivation system had a marked effect on the level of mycorrhizal colonisation. In pine, the highest level of colonisation (48%) was observed in bare-root systems, while in spruce, colonisation was highest in polyethylene rolls (71%). Direct internal transcribed spacer ribosomal DNA sequencing and isolation detected a total of 93 fungal taxa, including 27 mycorrhizal. A total of 71 (76.3%) fungi were identified at least to a genus level. The overlap between the two methods was low. Only 13 (13.9%) of taxa were both sequenced and isolated, 47 (50.5%) were detected exclusively by sequencing and 33 (35.5%) exclusively by isolation. All isolated mycorrhizal fungi were also detected by direct sequencing. Characteristic mycorrhizas were Phialophora finlandia, Amphinema byssoides, Rhizopogon rubescens, Suillus luteus and Thelephora terrestris. There was a moderate similarity in mycorrhizal communities between pine and spruce and among different cultivation systems.

Seasonal Dynamics of Arbuscular Mycorrhizal Fungal Communities in Roots in a Seminatural Grassland

ABSTRACT Symbiotic arbuscular mycorrhizal fungi (AMF) have been shown to influence both the diversity and productivity of grassland plant communities. These effects have been postulated to depend on the differential effects of individual mycorrhizal taxa on different plant species; however, so far there are few detailed studies of the dynamics of AMF colonization of different plant species. In this study, we characterized the communities of AMF colonizing the roots of two plant species, Prunella vulgaris and Antennaria dioica, in a Swedish seminatural grassland at different times of the year. The AMF small subunit rRNA genes were subjected to PCR, cloning, sequencing, and phylogenetic analysis. Nineteen discrete sequence types belonging to Glomus groups A and B and to the genus Acaulospora were distinguished. No significant seasonal changes in the species compositions of the AMF communities as a whole were observed. However, the two plant species hosted significantly different AMF communities. P. vulgaris hosted a rich AMF community throughout the entire growing season. The presence of AMF in A. dioica decreased dramatically in autumn, while an increased presence of Ascomycetes species was detected.