Trait-based assembly of arbuscular mycorrhizal fungal communities determines soil carbon formation and retention.

Fungi are crucial for soil organic carbon (SOC) formation, especially for the more persistent mineral-associated organic C (MAOC) pool. Yet, evidence for this often overlooks arbuscular mycorrhizal fungi (AMF) communities and how their composition and traits impact SOC accumulation. We grew sudangrass with AMF communities representing different traits conserved at the family level: competitors, from the Gigasporaceae family; ruderals, from the Glomeraceae family; or both families combined. We labeled sudangrass with 13 C-CO2 to assess AMF contributions to SOC, impacts on SOC priming, and fungal biomass persistence in MAOC. Single-family AMF communities decreased total SOC by 13.8%, likely due to fungal priming. Despite net SOC losses, all AMF communities contributed fungal C to soil but only the Glomeraceae community initially contributed to MAOC. After a month of decomposition, both the Glomeraceae and mixed-family communities contributed to MAOC formation. Plant phosphorus uptake, but not hyphal chemistry, was positively related to AMF soil C and MAOC accumulation. Arbuscular mycorrhizal fungi contribution to MAOC is dependent on the specific traits of the AMF community and related to phosphorus uptake. These findings provide insight into how variations in AMF community composition and traits, and thus processes like environmental filtering of AMF, may impact SOC accumulation.

A trait-based understanding of wood decomposition by fungi.

As the primary decomposers of organic material in terrestrial ecosystems, fungi are critical agents of the global carbon cycle. Yet our ability to link fungal community composition to ecosystem functioning is constrained by a limited understanding of the factors accounting for different wood decomposition rates among fungi. Here we examine which traits best explain fungal decomposition ability by combining detailed trait-based assays on 34 saprotrophic fungi from across North America in the laboratory with a 5-y field study comprising 1,582 fungi isolated from 74 decomposing logs. Fungal growth rate (hyphal extension rate) was the strongest single predictor of fungal-mediated wood decomposition rate under laboratory conditions, and accounted for up to 27% of the in situ variation in decomposition in the field. At the individual level, decomposition rate was negatively correlated with moisture niche width (an indicator of drought stress tolerance) and with the production of nutrient-mineralizing extracellular enzymes. Together, these results suggest that decomposition rates strongly align with a dominance-tolerance life-history trade-off that was previously identified in these isolates, forming a spectrum from slow-growing, stress-tolerant fungi that are poor decomposers to fast-growing, highly competitive fungi with fast decomposition rates. Our study illustrates how an understanding of fungal trait variation could improve our predictive ability of the early and midstages of wood decay, to which our findings are most applicable. By mapping our results onto the biogeographic distribution of the dominance-tolerance trade-off across North America, we approximate broad-scale patterns in intrinsic fungal-mediated wood decomposition rates.

Arbuscular mycorrhizal fungal communities with contrasting life-history traits influence host nutrient acquisition.

Life-history traits differ substantially among arbuscular mycorrhizal (AM) fungal families, potentially affecting hyphal nutrient acquisition efficiency, host nutrition, and thereby plant health and ecosystem function. Despite these implications, AM fungal community life-history strategies and community trait diversity effects on host nutrient acquisition are poorly understood. To address this knowledge gap, we grew sudangrass with AM fungal communities representing contrasting life-history traits and diversity: either (1) five species in the AM family Gigasporaceae, representing competitor traits, (2) five Glomerales species, representing ruderal traits, or (3) a mixed-trait community combining all ten AM fungal species. After 12 weeks, we measured above and belowground plant biomass and aboveground nutrient uptake and concentration. Overall, AM fungal colonization increased host nutrition, biomass, and foliar δ5nitrogen enrichment compared to the uncolonized control. Between the single-trait communities, the Glomeraceae community generally outperformed the Gigasporaceae community in host nutrition and plant growth, increasing plant phosphorus (P) uptake 1.5 times more than the Gigasporaceae community. We saw weak evidence for a synergistic effect of the mixed community, which was only higher for plant P concentration (1.26 times higher) and root colonization (1.26 times higher) compared to the single-trait communities. However, this higher P concentration did not translate to more P uptake or the highest plant biomass for the mixed community. These findings demonstrate that the AM symbiosis is affected by community differences at high taxonomic levels and provide insight into how different AM fungal communities and their associated traits affect host nutrition for fast-growing plant species.

Phylogenetic conservatism of mycoparasitism and its contribution to pathogen antagonism.

Closely related species are expected to have similar functional traits due to shared ancestry and phylogenetic inertia. However, few tests of this hypothesis are available for plant-associated fungal symbionts. Fungal leaf endophytes occur in all land plants and can protect their host plant from disease by a variety of mechanisms, including by parasitizing pathogens (e.g., mycoparasitism). Here, we tested whether phylogenetic relatedness among species of Cladosporium, a widespread genus that includes mycoparasitic species, predicts the effect of this endophyte on the severity of leaf rust disease. First, we used congruence among different marker sequences (i.e., genealogical concordance phylogenetic species recognition criterion) to delimit species of Cladosporium. Next, in a controlled experiment, we quantified both mycoparasitism and disease modification for the selected Cladosporium species. We identified 17 species of Cladosporium; all the species reduced rust disease severity in our experiment. Cladosporium phylogeny was a significant predictor of mycoparasitism. However, we did not observe a phylogenetic effect on disease severity overall, indicating that other mechanism/s operating independently of shared ancestry also contributed to endophyte effects on disease severity. Indeed, a second experiment showed that Cladosporium endophyte exudates (no live organism) from divergent species groups equally reduced disease severity. Our results reveal that multiple mechanisms contribute to the protective effects of an endophyte against a plant pathogen, but not all traits underlying these mechanisms are phylogenetically conserved.

Grazing Intensity Rather than Host Plant's Palatability Shapes the Community of Arbuscular Mycorrhizal Fungi in a Steppe Grassland.

Arbuscular mycorrhizal fungi (AMF) are the predominant type of mycorrhizal fungi in roots and rhizosphere soil of grass species worldwide. Grasslands are currently experiencing increasing grazing pressure, but it is not yet clear how grazing intensity and host plant grazing preference by large herbivores interact with soil- and root-associated AMF communities. Here, we tested whether the diversity and community composition of AMF in the roots and rhizosphere soil of two dominant perennial grasses, grazed differently by livestock, change in response to grazing intensity. We conducted a study in a long-term field experiment in which seven levels of field-manipulated grazing intensities were maintained for 13 years in a typical steppe grassland in northern China. We extracted DNA from the roots and rhizosphere soil of two dominant grasses, Leymus chinense (Trin.) Tzvel. and Stipa grandis P. Smirn, with contrasting grazing preference by sheep. AMF DNA from root and soil samples was then subjected to molecular analysis. Our results showed that AMF α-diversity (richness) at the virtual taxa (VT) level varied as a function of grazing intensity. Different VT showed completely different responses along the gradient, one increasing, one decreasing, and others showing no response. Glomeraceae was the most abundant AMF family along the grazing gradient, which fits well with the theory of disturbance tolerance of this group. In addition, sheep-grazing preference for host plants did not explain much of the variation in AMF α-diversity. However, the two grass species exhibited different AMF community composition in their roots and rhizosphere soils. Roots exhibited a lower α-diversity and higher ß-diversity within the AMF community than soils. Overall, our results suggest that long-term grazing intensity might have changed the abundance of functionally diverse AMF taxa in favor of those with disturbance-tolerant traits. We suggest our results would be useful in informing the choice of mycorrhizal fungi indicator variables when assessing the impacts of grassland management choices on grassland ecosystem functioning.

Global analysis reveals an environmentally driven latitudinal pattern in mushroom size across fungal species.

Although macroecology is a well-established field, much remains to be learned about the large-scale variation of fungal traits. We conducted a global analysis of mean fruit body size of 59 geographical regions worldwide, comprising 5340 fungal species exploring the response of fruit body size to latitude, resource availability and temperature. The results showed a hump-shaped relationship between mean fruit body size and distance to the equator. Areas with large fruit bodies were characterised by a high seasonality and an intermediate mean temperature. The responses of mutualistic species and saprotrophs were similar. These findings support the resource availability hypothesis, predicting large fruit bodies due to a seasonal resource surplus, and the thermoregulation hypothesis, according to which small fruit bodies offer a strategy to avoid heat and cold stress and therefore occur at temperature extremes. Fruit body size may thus be an adaptive trait driving the large-scale distribution of fungal species.

Taxi drivers: the role of animals in transporting mycorrhizal fungi.

Dispersal of mycorrhizal fungi via animals and the importance for the interacting partners' life history as well as for ecosystems is an understudied topic. In this review, we describe the available evidence and the most important knowledge gaps and finally suggest ways to gain the missing information. So far, 33 articles have been published proving a successful transfer of mycorrhizal propagules by animals. The vast majority of research on invertebrates was focused on arbuscular mycorrhizal (AM) fungi, whereas papers on vertebrates (mainly rodents and artiodactyls) equally addressed ectomycorrhizal (ECM) and AM fungi. Effective dispersal has been mostly shown by the successful inoculation of bait plants and less commonly by spore staining or germination tests. Based on the available data and general knowledge on animal lifestyles, collembolans and oribatid mites may be important in transporting ECM fungal propagules by ectozoochory, whereas earthworms, isopods, and millipedes could mainly transfer AM fungal spores in their gut systems. ECM fungal distribution may be affected by mycophagous dipterans and their hymenopteran parasitoids, while slugs, snails, and beetles could transport both mycorrhizal groups. Vertebrates feeding on fruit bodies were shown to disperse mainly ECM fungi, while AM fungi are transported mostly accidentally by herbivores. The important knowledge gaps include insufficient information on dispersal of fungal propagules other than spores, the role of invertebrates in the dispersal of mycorrhizal fungi, the way in which propagules pass through food webs, and the spatial distances reached by different dispersal mechanisms both horizontally and vertically.

Toward Modeling the Resistance and Resilience of "Below-ground" Fungal Communities: A Mechanistic and Trait-Based Approach.

The role of fungi in shaping ecosystems is well evidenced and there is growing recognition of their importance among scientists and the general public. Establishing and separating the role of key local (soil chemical, biological, and physical properties) and global (climate, dispersal limitation) drivers in fungal community structure and functioning is currently a source of frustration to mycologists. The quest to determine niche processes and environmental characteristics shaping fungal community structure, known to be important for plant and animal communities, is proving difficult, resulting in the acknowledgment that niche neutral processes (climate, dispersal limitations) may dominate. The search for predictable patterns in fungal community structure may have been restricted as the "appropriate" scales at which to measure community structure and characterize the environment have not been fully determined yet, and the focus on taxonomy makes it difficult to link environmental characteristics to fungal traits. While key determinants of microbial community composition have been uncovered for some functional groups, the differential response of functional groups is largely unknown. Before we can truly understand what drives the development of microbial community structure, an understanding of the autecology of major fungal taxa and how they interact with their immediate environment (from the micro- up to kilometer scale) is urgently needed. Furthermore, key information and empirical data is missing at the microscale due to experimental difficulties in mapping this heterogeneous and opaque environment. We therefore present a framework that would help generate this much-needed empirical data and information at the microscale, together with modeling approaches to link the spatial and temporal scales. The latter is important as we propose that there is much to be gained by linking our understanding of fungal community responses across scales, in order to develop species and community-environment-function predictive models.

Fungal traits help to understand the decomposition of simple and complex plant litter.

Litter decomposition is a key ecosystem process, relevant for the release and storage of nutrients and carbon in soil. Soil fungi are one of the dominant drivers of organic matter decomposition, but fungal taxa differ substantially in their functional ability to decompose plant litter. Knowledge is mostly based on observational data and subsequent molecular analyses and in vitro studies have been limited to forest ecosystems. In order to better understand functional traits of saprotrophic soil fungi in grassland ecosystems, we isolated 31 fungi from a natural grassland and performed several in vitro studies testing for i) leaf and wood litter decomposition, ii) the ability to use carbon sources of differing complexity, iii) the enzyme repertoire. Decomposition strongly varied among phyla and isolates, with Ascomycota decomposing the most and Mucoromycota decomposing the least. The phylogeny of the fungi and their ability to use complex carbon were the most important predictors for decomposition. Our findings show that it is crucial to understand the role of individual members and functional groups within the microbial community. This is an important way forward to understand the role of microbial community composition for the prediction of litter decomposition and subsequent potential carbon storage in grassland soils.

What are mycorrhizal traits?

Traits are inherent properties of organisms, but how are they defined for organismal networks such as mycorrhizal symbioses? Mycorrhizal symbioses are complex and diverse belowground symbioses between plants and fungi that have proved challenging to fit into a unified and coherent trait framework. We propose an inclusive mycorrhizal trait framework that classifies traits as morphological, physiological, and phenological features that have functional implications for the symbiosis. We further classify mycorrhizal traits by location - plant, fungus, or the symbiosis - which highlights new questions in trait-based mycorrhizal ecology designed to charge and challenge the scientific community. This new framework is an opportunity for researchers to interrogate their data to identify novel insights and gaps in our understanding of mycorrhizal symbioses.