Microbial succession on decomposing root litter in a drought-prone Scots pine forest

Herzog, Claude; Hartmann, Martin; Frey, Beat; Stierli, Beat; Rumpel, Cornélia; Buchmann, Nina; Brunner, Ivano

doi:10.1038/s41396-019-0436-6

Cited by 94 publications

(67 citation statements)

References 130 publications

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“…After transplantation, fast-growing Ascomycota dominated, and then were replaced by earlystage ectomycorrhizal fungi. Previous studies looked at the mycorrhizal succession in pine seedlings (Peay et al, 2011;Herzog et al, 2019;Rudawska et al, 2019), and we found that the shift of root associated fungi in our study followed the general trend, despite being inoculated with T. matsutake.…”

Section: Change Of Fungal Communities In Pine Seedlings After Transplsupporting

confidence: 70%

Successional Change of the Fungal Microbiome Pine Seedling Roots Inoculated With Tricholoma matsutake

Park

Yoo

et al. 2020

Front. Microbiol.

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The pine mushroom (Tricholoma matsutake; Agaricales, Tricholomataceae) is an ectomycorrhizal fungus that produces a commercially valuable, edible mushrooms. Attempts to artificially cultivate T. matsutake has so far been unsuccessful. One method used to induce T. matsutake to produce fruiting bodies of in the wild is shiro (mycelial aggregations of T. matsutake) transplantation. In vitro ectomycorrhization of T. matsutake with seedlings of Pinus densiflora has been successful, but field trials showed limited production of fruiting bodies. Few studies have been done to test what happens after transplantation in the wild, whether T. matsutake persists on the pine seedling roots or gets replaced by other fungi. Here, we investigated the composition and the interaction of the root fungal microbiome of P. densiflora seedlings inoculated with T. matsutake over a 3 year period after field transplantation, using high-throughput sequencing. We found a decline of T. matsutake colonization on pine roots and succession of mycorrhizal fungi as P. densiflora seedlings grew. Early on, roots were colonized by fast-growing, saprotrophic Ascomycota, then later replaced by early stage ectomycorrhiza such as Wilcoxina. At the end, more competitive Suillus species dominated the host roots. Most of the major OTUs had negative or neutral correlation with T. matsutake, but several saprotrophic/plant pathogenic/mycoparasitic species in genera Fusarium, Oidiodendron, and Trichoderma had positive correlation with T. matsutake. Four keystone species were identified during succession; two species (Fusarium oxysporum, and F. trincintum) had a positive correlation with T. matsutake, while the other two had a negative correlation (Suillus granulatus, Cylindrocarpon pauciseptatum). These findings have important implications for further studies on the artificial cultivation of T. matsutake.

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Section: Change Of Fungal Communities In Pine Seedlings After Transplsupporting

confidence: 70%

Successional Change of the Fungal Microbiome Pine Seedling Roots Inoculated With Tricholoma matsutake

Park

Yoo

et al. 2020

Front. Microbiol.

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“…Indeed, microbe-derived functions, such as metabolites in this study, directly translate to human applications ( 47 ). The link between taxonomic and functional changes has previously been observed also in other systems such as in soils ( 48 , 49 ). As such, it is of great significance to study community differences and link them to functioning to evaluate the functional consequences of observed community changes in any studied system.…”

Section: Discussionmentioning

confidence: 54%

“…Thus, it is helpful to simplify complex communities into individual taxa to determine and focus subsequent analyses on functionally important keystone species ( 59 , 60 ). In comparison to commonly performed whole-community analyses ( 8 , 48 , 61 ), the method based on indicator microorganisms and metabolites can accurately reflect changes in environmental conditions. Our indicator taxon approach to determine the key factors driving community and functional changes not only could reveal differences much more strongly but even allowed accurate modeling of temporal changes in taxonomically important microorganisms and functional metabolites.…”

Section: Discussionmentioning

confidence: 99%

Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System

et al. 2020

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We are rapidly increasing our understanding on the spatial distribution of microbial communities. However, microbial functioning, as well as temporal differences and mechanisms causing microbial community shifts, remains comparably little explored. Here, using Chinese liquor fermentation as a model system containing a low microbial diversity, we studied temporal changes in microbial community structure and functioning. For that, we used high-throughput sequencing to analyze the composition of bacteria and fungi and analyzed the microbially derived metabolome throughout the fermentation process in all four seasons in both 2018 and 2019. We show that microbial communities and the metabolome changed throughout the fermentation process in each of the four seasons, with metabolome diversity increasing throughout the fermentation process. Across seasons, bacterial and fungal communities as well as the metabolome driven by 10 indicator microorganisms and six metabolites varied even more. Daily average temperature in the external surroundings was the primary determinant of the observed temporal microbial community and metabolome changes. Collectively, our work reveals critical insights into patterns and processes determining temporal changes of microbial community composition and functioning. We highlight the importance of linking taxonomic to functional changes in microbial ecology to enable predictions of human-relevant applications. IMPORTANCE We used Chinese liquor fermentation as a model system to show that microbiome composition changes more dramatically across seasons than throughout the fermentation process within seasons. These changes translate to differences in the metabolome as the ultimate functional outcome of microbial activity, suggesting that temporal changes in microbiome composition are translating into functional changes. This result is striking as it suggests that microbial functioning, despite controlled conditions in the fermentors, fluctuates over season along with external temperature differences, which threatens a reproducible food taste. As such, we believe that our study provides a stepping-stone into novel taxonomy-functional studies that promote future work in other systems and that also is relevant in applied settings to better control surrounding conditions in food production.

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“…(b) root exudates are also an important source of organic carbon input into soil, especially in actively growing plants (De Deyn, Cornelissen, & Bardgett, 2008;Herzog et al, 2019); (c) greater plant coverage decreases carbon loss by wind erosion (Zhou, Li, Chen, Zhang, & Li, 2011). Previous studies have shown that the richness loss of specific bacterial and eukaryotic taxa can further increase the growth of a few fast-growing and more competitive microbes (Fierer et al, 2012;Fierer, Bradford, & Jackson, 2007;Li, Rui, Mao, Yannarell, & Mackie, 2014).…”

Section: Fencing Increased Bacterial and Eukaryotic Abundancementioning

confidence: 99%

Fencing decreases microbial diversity but increases abundance in grassland soils on the Tibetan Plateau

et al. 2020

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Fencing usually increases soil organic carbon and nutrients and eventually enhances soil microbial diversity; however with different or even conflicting results, the mechanisms underlying the diversity reduction remain unclear. Aiming to reveal the mechanism of diversity reduction, we explored the soil microbial diversity and community structure in fenced areas (5-and 10-years enclosure) and grazing during a growing season in arid and semiarid steppe, using Illumina sequencing of 16S and 18S rRNA genes. The results revealed that fencing and season both substantially increased soil total organic carbon (TOC), while the enhancing TOC substantially reduced soil pH. Fencing significantly increased soil bacterial and eukaryotic abundance due to the enhancing TOC, which was indicated by positive correlation (p < .05). Contrastingly, fencing significantly decreased soil bacterial and eukaryotic diversity. Our results further revealed that fencing-and season-driven change in soil water content and soil pH played key roles in reducing the bacterial and eukaryotic diversity, respectively. Distance-based linear model demonstrated that fencing dominantly drove the soil bacterial and eukaryotic community variations by explaining 15.64 and 24.88%, respectively, and redundancy analysis showed that the fencing effect was dependent on growing months. Bacteria were dominated by Cyanobacteria and Proteobacteria, and eukaryotes were dominated by Streptophyta, Ascomycota and Basidiomycota. Cyanobacteria relative abundance remained stable from May to September in fencing but substantially increased in grazing. Our findings offer a new insight into the mechanism of the soil microbial diversity reduction, and reveal the season-dependency of fencing effect in arid and semiarid grasslands.

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Microbial succession on decomposing root litter in a drought-prone Scots pine forest

Cited by 94 publications

References 130 publications

Successional Change of the Fungal Microbiome Pine Seedling Roots Inoculated With Tricholoma matsutake

Successional Change of the Fungal Microbiome Pine Seedling Roots Inoculated With Tricholoma matsutake

Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System

Fencing decreases microbial diversity but increases abundance in grassland soils on the Tibetan Plateau

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