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Long-Term Compost Amendment Spurs Cellulose Decomposition by Driving Shifts in Fungal Community Composition and Promoting Fungal Diversity and Phylogenetic Relatedness.

ABSTRACT: Cellulose is the most abundant polysaccharide in plant biomass and an important precursor of soil organic matter formation. Fungi play a key role in carbon cycling dynamics because they tend to decompose recalcitrant materials. Here, we applied [¹²C]cellulose and [¹³C]cellulose to distinguish the effects of application of compost, nitrogen-phosphorus-potassium (NPK) fertilizer, and no fertilizer (control) for 27 years upon cellulose decomposition via RNA-based stable isotope probing (RNA-SIP). The loss ratio of added cellulose C in compost soil was 67.6 to 106.7% higher than in NPK and control soils during their 20-day incubation. Dothideomycetes (mainly members of the genus Cryptococcus) dominated cellulose utilization in compost soil, whereas the copiotrophic Sordariomycetes were more abundant in NPK and unfertilized soils. Compared with NPK and control soils, compost application increased the diversity of ¹³C-assimilating fungi. The ¹³C-labeled fungal communities in compost soil were more phylogenetically clustered and exhibited greater species relatedness than those in NPK and control soils, perhaps because of stringent filtering of narrow-spectrum organic resources and biological invasion originating from added compost. These changes led to an augmented decomposition capacity of fungal species for cellulose-rich substrates and reduced cellulose C sequestration efficiency. The RNA-SIP technique is more sensitive to responses of fungi to altered soil resource availability than DNA-SIP. Overall, long-term compost application modified fungal community composition and promoted fungal diversity and phylogenetic relatedness, accelerating the decomposition of substrate cellulose in soil. This work also highlights the RNA-SIP technique's value for comprehensively assessing the contributions of active fungi to the substrate decomposition process. IMPORTANCE Cellulose is a very rich component in plant biomass and an important precursor of soil organic matter formation. Fungal communities are known to be important drivers of organic carbon accumulation in arable soils. However, current understanding of responses of fungal species to cellulose amendment and the contributions of active fungi to substrate decomposition process is still very superficial. Here, we established a [¹³C]cellulose microcosm experiment with soils subjected to long-term application of compost, nitrogen-phosphorus-potassium (NPK) fertilizer, and no fertilizer (control). The novel ¹³C-RNA-SIP technique with subsequent high-throughput sequencing was used to investigate the linkages between active fungal taxa and cellulose decomposition. Our study demonstrated that Dothideomycetes dominated cellulose utilization in compost soil, whereas the copiotrophic Sordariomycetes were more enriched in both NPK and unfertilized soils. We also found that the compost amendment promoted fungal diversity and phylogenetic relatedness and strengthened the decomposition capacity of fungi for cellulose-rich substrates by enhancing synergistic interactions, thereby reducing cellulose C sequestration efficiency. Overall, our research has implications for our understanding of the role of active fungi in cellulose C transformation in soils undergoing different types of long-term nutrient management.

SUBMITTER: Miao Y

PROVIDER: S-EPMC9239258 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Until recently, many phytoremediation studies were focused solely on a plants ability to reclaim heavy metal (HM) polluted soil through a range of different processes, such as phytoextraction and phytostabilization. However, the interaction between plants and their own rhizosphere microbiome represents a new research frontier for phytoremediation. Our hypothesis is that rhizomicrobiome might play a key role in plant wellness and in the response to external stimuli; therefore, this study aimed to shed light the rhizomicrobiome dynamics after an organic amendment (e.g., compost) and/or HM pollution (e.g., Zn), and its relation with plant reclamation ability. To reach this goal we set up a greenhouse experiment cultivating in pot an elite black poplar clone (N12) selected in the past for its excellent ability to reclaim heavy metals. N12 saplings were grown on a soil amended with compost and/or spiked with high Zn doses. At the end of the experiment, we observed that the compost amendment strongly increased the foliar size but did not affect significantly the Zn accumulation in plant. Furthermore, the rhizomicrobiome communities (bacteria and fungi), investigated through NGS, highlighted how α diversity increased in all treatments compared to the untreated N12 saplings. Soil compost amendment, as well as Zn pollution, strongly modified the bacterial rhizomicrobiome structure. Conversely, the variation of the fungal rhizomicrobiome was only marginally affected by soil Zn addition, and only partially impaired by compost. Nevertheless, substantial alterations of the fungal community were due to both compost and Zn. Together, our experimental results revealed that organic amendment increased the bacterial resistance to external stimuli whilst, in the case of fungi, the amendment made the fungi microbiome more susceptible. Finally, the greater microbiome biodiversity does not imply, in this case, a better plant wellness or phytoremediation ability, although the microbiome plays a role in the external stimuli response supporting plant life.

Project description:Microorganisms drive litter decomposition while maintaining the chemical cycle of ecosystems. We used the dominant vegetation (Imperata cylindrica) in the mining area selected for this study for this experiment to explore fungal community characteristics, key fungal groups, and their associative driving factors during I. cylindrica litter decomposition. Maximum litter C/N values occurred 100days after the commencement of the decomposition experiment during all different recovery years in this copper tailings area. Heavy metals in litter [copper (Cu), zinc (Zn), plumbum (Pb), and cadmium (Cd)] accumulated gradually with decomposition. The dominant fungal phyla observed in the community were Ascomycota and Basidiomycota, while the classes Sordariomycetes and Eurotiomycetes significantly increased as litter decomposition progressed. Degrees of connectivity and interaction between fungal communities were highest during the early litter decomposition stage. Sordariomycetes, Dothideomycetes, and Leotiomycetes all played critical roles in maintaining fungal community relationships. The effect of physicochemical properties and enzyme activities in I. cylindrica litter was significant on the dominant fungi, while driving factors that affected fungal communities differed over different recovery stages. Total nitrogen (TN), heavy metals, pH, and enzyme activities in the little were significantly correlated with fungal community composition. Litter properties throughout the litter decomposition process mainly affected the dynamics of the fungal community structure. The main environmental factors that affected fungal community structure were copper content and pH. Dichotomopilus, Trichoderma, Knufia, Phialophora, Oxyporus, and Monocillium, which all played important roles in litter decomposition, positively correlated with heavy metals, sucrase, and catalase. Finally, results from this study will help us better clarify litter decomposition mechanisms in degraded ecosystems as well as provide a scientific basis for improving species cycling and nutrient transformation efficiency in mining ecosystems.

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Long-Term Compost Amendment Spurs Cellulose Decomposition by Driving Shifts in Fungal Community Composition and Promoting Fungal Diversity and Phylogenetic Relatedness.

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