What determines transfer of carbon from plants to mycorrhizal fungi?

Biological Market Models are common evolutionary frameworks to understand the maintenance of mutualism in mycorrhizas. 'Surplus C' hypotheses provide an alternative framework where stoichiometry and source-sink dynamics govern mycorrhizal function. A critical difference between these frameworks is whether carbon transfer from plants is regulated by nutrient transfer from fungi or through source-sink dynamics. In this review, we: provide a historical perspective; summarize studies that asked whether plants transfer more carbon to fungi that transfer more nutrients; conduct a meta-analysis to assess whether mycorrhizal plant growth suppressions are related to carbon transfer; and review literature on cellular mechanisms for carbon transfer. In sum, current knowledge does not indicate that carbon transfer from plants is directly regulated by nutrient delivery from fungi. Further, mycorrhizal plant growth responses were linked to nutrient uptake rather than carbon transfer. These findings are more consistent with 'Surplus C' hypotheses than Biological Market Models. However, we also identify research gaps, and future research may uncover a mechanism directly linking carbon and nutrient transfer. Until then, we urge caution when applying economic terminology to describe mycorrhizas. We present a synthesis of ideas, consider knowledge gaps, and suggest experiments to advance the field.

Surplus Carbon Drives Allocation and Plant-Soil Interactions.

Plant growth is usually constrained by the availability of nutrients, water, or temperature, rather than photosynthetic carbon (C) fixation. Under these conditions leaf growth is curtailed more than C fixation, and the surplus photosynthates are exported from the leaf. In plants limited by nitrogen (N) or phosphorus (P), photosynthates are converted into sugars and secondary metabolites. Some surplus C is translocated to roots and released as root exudates or transferred to root-associated microorganisms. Surplus C is also produced under low moisture availability, low temperature, and high atmospheric CO2 concentrations, with similar below-ground effects. Many interactions among above- and below-ground ecosystem components can be parsimoniously explained by the production, distribution, and release of surplus C under conditions that limit plant growth.

Limited Effects of Variable-Retention Harvesting on Fungal Communities Decomposing Fine Roots in Coastal Temperate Rainforests.

Fine root litter is the principal source of carbon stored in forest soils and a dominant source of carbon for fungal decomposers. Differences in decomposer capacity between fungal species may be important determinants of fine-root decomposition rates. Variable-retention harvesting (VRH) provides refuge for ectomycorrhizal fungi, but its influence on fine-root decomposers is unknown, as are the effects of functional shifts in these fungal communities on carbon cycling. We compared fungal communities decomposing fine roots (in litter bags) under VRH, clear-cut, and uncut stands at two sites (6 and 13 years postharvest) and two decay stages (43 days and 1 year after burial) in Douglas fir forests in coastal British Columbia, Canada. Fungal species and guilds were identified from decomposed fine roots using high-throughput sequencing. Variable retention had short-term effects on ß-diversity; harvest treatment modified the fungal community composition at the 6-year-postharvest site, but not at the 13-year-postharvest site. Ericoid and ectomycorrhizal guilds were not more abundant under VRH, but stand age significantly structured species composition. Guild composition varied by decay stage, with ruderal species later replaced by saprotrophs and ectomycorrhizae. Ectomycorrhizal abundance on decomposing fine roots may partially explain why fine roots typically decompose more slowly than surface litter. Our results indicate that stand age structures fine-root decomposers but that decay stage is more important in structuring the fungal community than shifts caused by harvesting. The rapid postharvest recovery of fungal communities decomposing fine roots suggests resiliency within this community, at least in these young regenerating stands in coastal British Columbia.IMPORTANCE Globally, fine roots are a dominant source of carbon in forest soils, yet the fungi that decompose this material and that drive the sequestration or respiration of this carbon remain largely uncharacterized. Fungi vary in their capacity to decompose plant litter, suggesting that fungal community composition is an important determinant of decomposition rates. Variable-retention harvesting is a forestry practice that modifies fungal communities by providing refuge for ectomycorrhizal fungi. We evaluated the effects of variable retention and clear-cut harvesting on fungal communities decomposing fine roots at two sites (6 and 13 years postharvest), at two decay stages (43 days and 1 year), and in uncut stands in temperate rainforests. Harvesting impacts on fungal community composition were detected only after 6 years after harvest. We suggest that fungal community composition may be an important factor that reduces fine-root decomposition rates relative to those of above-ground plant litter, which has important consequences for forest carbon cycling.

Relationships among leaf functional traits, litter traits, and mass loss during early phases of leaf litter decomposition in 12 woody plant species.

Litter 'quality' or decomposability has historically been estimated through measuring chemical attributes, such as concentrations of nitrogen or 'lignin'. More recently, foliar functional traits, which may incorporate indications of the physical structures of tissues, have been found to correlate with litter mass loss rates. However, these traits may not be adequate to predict early rates of mass loss, in which two factors are crucial: the amount of material quickly lost through leaching, and the ease of access of decomposer organisms to the more labile tissues in the interior of the litter. We investigated relationships among physical and chemical traits in foliage and litter of 12 species native to British Columbia and then observed how these traits related to mass loss during the first 3 months (Phase I) and between 3 and 12 months (Phase II). Novel traits measured in this study include cuticle thickness, litter leaching loss, and litter water uptake. Foliar and litter traits both co-varied along spectra, but several chemical traits, such as nitrogen concentration, changed from foliage to litter, i.e., during senescence. Phase I mass loss was best predicted by leaching loss and traits relating to leaching, such as cuticle thickness and specific leaf area. Phase II mass loss was predicted by traits that may relate to decomposer access and activity, such as leaf dry matter content and foliar nitrogen. Physical traits predicted mass loss as well or better than chemical traits, suggesting that physical characteristics of litter are important in determining early rates of decomposition.

Plant Community and Nitrogen Deposition as Drivers of Alpha and Beta Diversities of Prokaryotes in Reconstructed Oil Sand Soils and Natural Boreal Forest Soils.

The Athabasca oil sand deposit is one of the largest single oil deposits in the world. Following surface mining, companies are required to restore soil-like profiles that can support the previous land capabilities. The objective of this study was to assess whether the soil prokaryotic alpha diversity (α-diversity) and ß-diversity in oil sand soils reconstructed 20 to 30 years previously and planted to one of three vegetation types (coniferous or deciduous trees and grassland) were similar to those found in natural boreal forest soils subject to wildfire disturbance. Prokaryotic α-diversity and ß-diversity were assessed using massively parallel sequencing of 16S rRNA genes. The ß-diversity, but not the α-diversity, differed between reconstructed and natural soils. Bacteria associated with an oligotrophic lifestyle were more abundant in natural forest soils, whereas bacteria associated with a copiotrophic lifestyle were more abundant in reconstructed soils. Ammonia-oxidizing archaea were most abundant in reconstructed soils planted with grasses. Plant species were the main factor influencing α-diversity in natural and in reconstructed soils. Nitrogen deposition, pH, and plant species were the main factors influencing the ß-diversity of the prokaryotic communities in natural and reconstructed soils. The results highlight the importance of nitrogen deposition and aboveground-belowground relationships in shaping soil microbial communities in natural and reconstructed soils.IMPORTANCE Covering over 800 km2, land disturbed by the exploitation of the oil sands in Canada has to be restored. Here, we take advantage of the proximity between these reconstructed ecosystems and the boreal forest surrounding the oil sand mining area to study soil microbial community structure and processes in both natural and nonnatural environments. By identifying key characteristics shaping the structure of soil microbial communities, this study improved our understanding of how vegetation, soil characteristics and microbial communities interact and drive soil functions.

Does exogenous carbon extend the realized niche of canopy lichens? Evidence from sub-boreal forests in British Columbia.

Foliose lichens with cyanobacterial bionts (bipartite and tripartite) form a distinct assemblage of epiphytes strongly associated with humid microclimatic conditions in inland British Columbia. Previous research showed that these cyano- and cephalolichen communities are disproportionately abundant and species-rich on conifer saplings beneath Populus compared to beneath other tree species. More revealing, lichens with cyanobacterial bionts were observed beneath Populus even in stands that did not otherwise support them. We experimentally test the hypothesis that this association is due to the interception of glucose-rich nectar that is exuded from Populus extra-floral nectaries (EFN). Using CO2 flux measurements and phospholipid fatty acid (PLFA) analysis with experimental applications of 13C6-labeled glucose, we demonstrate that cyano- and cephalolichens have a strong respiratory response to glucose. Lichens treated with glucose had lower net photosynthesis and higher establishment rates than control thalli. Furthermore, lichens with cyanobacterial bionts rapidly incorporate exogenous 13C into lichen fatty acid tissues. A large proportion of the 13C taken up by the lichens was incorporated into fungal biomarkers, suggesting that the mycobiont absorbed and assimilated the majority of applied 13C6 glucose. Our observations suggest that both cyanolichens and cephalolichens may utilize an exogenous source of glucose, made available by poplar EFNs. The exogenous C may enable these lichens to become established by providing a source of C for fungal respiration despite drought-induced inactivity of the cyanobacterial partner. As such, the mycobiont may adopt an alternative nutritional strategy, using available exogenous carbon to extend its realized niche.

Organic and inorganic nitrogen nutrition of western red cedar, western hemlock and salal in mineral N-limited cedar-hemlock forests.

Western red cedar (Thuja plicata Donn.), western hemlock (Tsuga heterophylla Raf. Sarge) and salal (Gaultheria shallon Pursh) are the main species growing in cedar-hemlock forests on Vancouver Island, Canada. Based on the dominance of organic N in these systems, we tested the hypotheses that: (1) organic N can be utilized by the three plant species; and (2) salal, which is ericoid mycorrhizal and has high tannin concentration in its tissues, would absorb more N from the complex organic N compounds than the other two species. The abilities of cedar, hemlock and salal to take up 15N,13C-labelled glutamic acid were measured and the capacities of the three species to use nitrate (NO3-), ammonium (NH4+), glutamic acid, protein and protein-tannin N were compared over a 20-day period. Based on 13C enrichment, all three species absorbed at least a portion of glutamic acid intact. Cedar, hemlock and salal also showed similar patterns of N uptake from the NO3-, NH4+, glutamic acid, protein and protein-tannin treatments. The largest proportions of applied N were taken up from the NO3- and NH4+ treatments while smaller amounts of N were absorbed from the organic N compounds. Thus organic N was accessed to a modest degree by all three species, and salal did not have a greater capacity to utilize protein and protein-tannin-N.

The influence of the forest canopy on nutrient cycling.

Rates of key soil processes involved in recycling of nutrients in forests are governed by temperature and moisture conditions and by the chemical and physical nature of the litter. The forest canopy influences all of these factors and thus has a large influence on nutrient cycling. The increased availability of nutrients in soil in clearcuts illustrates how the canopy retains nutrients (especially N) on site, both by storing nutrients in foliage and through the steady input of available C in litter. The idea that faster decomposition is responsible for the flush of nitrate in clearcuts has not been supported by experimental evidence. Soil N availability increases in canopy gaps as small as 0.1 ha, so natural disturbances or partial harvesting practices that increase the complexity of the canopy by creating gaps will similarly increase the spatial variability in soil N cycling and availability within the forest. Canopy characteristics affect the amount and composition of leaf litter produced, which largely determines the amount of nutrients to be recycled and the resulting nutrient availability. Although effects of tree species on soil nutrient availability were thought to be brought about largely through differences in the decomposition rate of their foliar litter, recent studies indicate that the effect of tree species can be better predicted from the mass and nutrient content of litter produced, hence total nutrient return, than from litter decay rate. The greater canopy complexity in mixed species forests creates similar heterogeneity in nutritional characteristics of the forest floor. Site differences in slope position, parent material and soil texture lead to variation in species composition and productivity of forests, and thus in the nature and amount of litter produced. Through this positive feedback, the canopy accentuates inherent differences in site fertility.