Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function

Koide, Roger T.; Fernandez, Christopher W.; Malcolm, Glenna M.

doi:10.1111/nph.12538

Cited by 203 publications

(223 citation statements)

References 60 publications

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“…Accordingly, it has been suggested that melanin contributes to C storage in soils (5), eventually accumulating as humic material (163,177,179). In consideration of these properties, Koide et al (42) proposed melanin production as a fungal trait that may form a direct link between environmental stress and ecosystem function.…”

Section: Stress Tolerancementioning

confidence: 99%

“…Although they can act as "decomposers in disguise" (reviewed in reference 249), their capacity for breakdown of complex organic C is relatively low (115,250). In addition, ectomycorrhizal root tips and rhizomorphs can be long-lived and slow to decompose (45,(251)(252)(253)(254)(255)(256)(257), which can contribute to microbial immobilization of C, N, and P. Altogether, mycorrhizal fungi may augment soil C storage (30,42,255,258,259). Moreover, their abundance is influenced not only directly by climate and nutrient availability but also by the presence and activities of host plants (260)(261)(262).…”

Section: Figmentioning

confidence: 99%

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Fungal Traits That Drive Ecosystem Dynamics on Land

Treseder

Lennon

2015

Microbiol Mol Biol Rev

442

322

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SUMMARY Fungi contribute extensively to a wide range of ecosystem processes, including decomposition of organic carbon, deposition of recalcitrant carbon, and transformations of nitrogen and phosphorus. In this review, we discuss the current knowledge about physiological and morphological traits of fungi that directly influence these processes, and we describe the functional genes that encode these traits. In addition, we synthesize information from 157 whole fungal genomes in order to determine relationships among selected functional genes within fungal taxa. Ecosystem-related traits varied most at relatively coarse taxonomic levels. For example, we found that the maximum amount of variance for traits associated with carbon mineralization, nitrogen and phosphorus cycling, and stress tolerance could be explained at the levels of order to phylum. Moreover, suites of traits tended to co-occur within taxa. Specifically, the genetic capacities for traits that improve stress tolerance—β-glucan synthesis, trehalose production, and cold-induced RNA helicases—were positively related to one another, and they were more evident in yeasts. Traits that regulate the decomposition of complex organic matter—lignin peroxidases, cellobiohydrolases, and crystalline cellulases—were also positively related, but they were more strongly associated with free-living filamentous fungi. Altogether, these relationships provide evidence for two functional groups: stress tolerators, which may contribute to soil carbon accumulation via the production of recalcitrant compounds; and decomposers, which may reduce soil carbon stocks. It is possible that ecosystem functions, such as soil carbon storage, may be mediated by shifts in the fungal community between stress tolerators and decomposers in response to environmental changes, such as drought and warming.

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Section: Stress Tolerancementioning

confidence: 99%

Section: Figmentioning

confidence: 99%

Fungal Traits That Drive Ecosystem Dynamics on Land

Treseder

Lennon

2015

Microbiol Mol Biol Rev

442

322

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“…EM fungi play a significant role in global nutrient and carbon cycles by enhancing the nutrient and water uptake by trees and absorbing carbon from their hosts (Smith and Read, 2008). Temperate and boreal forests, which cover B14% of the land surface (FAO, 2012), harbor hundreds of taxonomically and functionally diverse EM fungi (Read and PerezMoreno, 2003;Tedersoo et al, 2010;Koide et al, 2014). Recent environmental change may have altered fungal communities, which would subsequently affect the associated plant communities and ecosystem functioning (Parrent et al, 2006;Johnson et al, 2013;Dickie et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains

et al. 2015

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Separating the effects of environmental factors and spatial distance on microbial composition is difficult when these factors covary. We examined the composition of ectomycorrhizal (EM) fungi along elevation gradients on geographically distant mountains to clarify the effect of climate at the regional scale. Soil cores were collected from various forest types along an elevation gradient in southwestern Japan. Fungal species were identified by the internal transcribed spacer regions of the rDNA using direct sequencing. The occurrence of fungal species in this study was compared with a previous study conducted on a mountain separated by B550 km. In total, we recorded 454 EM fungi from 330 of 350 soil cores. Forty-seven fungal species (B20% of the total excluding singletons) were shared between two mountains, mostly between similar forest types on both mountains. Variation partitioning in redundancy analysis revealed that climate explained the largest variance in EM fungal composition. The similarity of forest tree composition, which is usually determined by climatic conditions, was positively correlated with the similarity of the EM fungal composition. However, the lack of large host effects implied that communities of forest trees and EM fungi may be determined independently by climate. Our data provide important insights that host plants and mutualistic fungi may respond to climate change idiosyncratically, potentially altering carbon and nutrient cycles in relation to the plant-fungus associations.

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“…Despite generally broad enzymatic capacities (6), not all ECM fungi have the ability to access peptide N, which has resulted in the classification of ECM fungi into "protein" and "nonprotein" species (7). Multiple authors have suggested that natural selection should favor traits allowing mycorrhizal fungi to utilize the most abundantly available N source in their environment (8). This would suggest that protein ECM fungal species have their ecological niche in organic-N-rich soils.…”

mentioning

confidence: 99%

Ectomycorrhizal Fungal Protein Degradation Ability Predicted by Soil Organic Nitrogen Availability

Rineau

Stas

Nguyen

et al. 2016

Appl Environ Microbiol

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In temperate and boreal forest ecosystems, nitrogen (N) limitation of tree metabolism is alleviated by ectomycorrhizal (ECM) fungi. As forest soils age, the primary source of N in soil switches from inorganic (NH 4 ؉ and NO 3 ؊ ) to organic (mostly proteins). It has been hypothesized that ECM fungi adapt to the most common N source in their environment, which implies that fungi growing in older forests would have greater protein degradation abilities. Moreover, recent results for a model ECM fungal species suggest that organic N uptake requires a glucose supply. To test the generality of these hypotheses, we screened 55 strains of 13 Suillus species with different ecological preferences for their in vitro protein degradation abilities. Suillus species preferentially occurring in mature forests, where soil contains more organic matter, had significantly higher protease activity than those from young forests with low-organic-matter soils or species indifferent to forest age. Within species, the protease activities of ecotypes from soils with high or low soil organic N content did not differ significantly, suggesting resource partitioning between mineral and organic soil layers. The secreted protease mixtures were strongly dominated by aspartic peptidases. Glucose addition had variable effects on secreted protease activity; in some species, it triggered activity, but in others, activity was repressed at high concentrations. Collectively, our results indicate that protease activity, a key ectomycorrhizal functional trait, is positively related to environmental N source availability but is also influenced by additional factors, such as carbon availability. In temperate and boreal forests, nitrogen (N) is the element that usually limits tree nutrition (1). To acquire sufficient N, trees form symbioses with microorganisms, including ectomycorrhizal (ECM) fungi (2), as well as shoot-endophytic bacteria (3). In soils, ECM fungi can take up N from both mineral and organic sources. Mineral N can be found as NH 4 ϩ or NO 3 Ϫ (4), while organic N can be present as part of several different organic oligomers or polymers: peptides, chitin, nucleic acids, and heterocyclic N compounds (3). Peptides are considered the dominant organic N source in forest soils (representing as much as 80% of organic N [5]), with ECM fungi typically retrieving N from this source through the use of proteases (3). Despite generally broad enzymatic capacities (6), not all ECM fungi have the ability to access peptide N, which has resulted in the classification of ECM fungi into "protein" and "nonprotein" species (7). Multiple authors have suggested that natural selection should favor traits allowing mycorrhizal fungi to utilize the most abundantly available N source in their environment (8). This would suggest that protein ECM fungal species have their ecological niche in organic-N-rich soils. Empirical support for this hypothesis has been shown by Lilleskov et al. (9), who found that ECM fungal species growing in a soil rich in mineral N had a lower a...

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Determining place and process: functional traits of ectomycorrhizal fungi that affect both community structure and ecosystem function

Cited by 203 publications

References 60 publications

Fungal Traits That Drive Ecosystem Dynamics on Land

Fungal Traits That Drive Ecosystem Dynamics on Land

Strong effect of climate on ectomycorrhizal fungal composition: evidence from range overlap between two mountains

Ectomycorrhizal Fungal Protein Degradation Ability Predicted by Soil Organic Nitrogen Availability

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