Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments

ABSTRACT The interactions between soil microbiomes at various trophic levels are essential for restoring soil functions. Legumes are considered as “pioneer crops” in degraded or contaminated soils because they can fix nitrogen through symbiotic relationships with rhizobacteria, which promotes soil f...

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Main Authors: Zhongyi Cheng, Jiachun Shi, Yan He, Yuxuan Chen, Youjing Wang, Xueling Yang, Tianyu Wang, Laosheng Wu, Jianming Xu
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.01049-22
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author Zhongyi Cheng
Jiachun Shi
Yan He
Yuxuan Chen
Youjing Wang
Xueling Yang
Tianyu Wang
Laosheng Wu
Jianming Xu
author_facet Zhongyi Cheng
Jiachun Shi
Yan He
Yuxuan Chen
Youjing Wang
Xueling Yang
Tianyu Wang
Laosheng Wu
Jianming Xu
author_sort Zhongyi Cheng
collection DOAJ
description ABSTRACT The interactions between soil microbiomes at various trophic levels are essential for restoring soil functions. Legumes are considered as “pioneer crops” in degraded or contaminated soils because they can fix nitrogen through symbiotic relationships with rhizobacteria, which promotes soil fertility. However, little is known about the abilities of legumes to contribute to the health of soil contaminated with cadmium (Cd). In this research, we applied a soil amendment (commercial Mg–Ca–Si conditioner, CMC) at two rates (1,500 and 3,000 kg/ha) in a Cd-contaminated soybean field. Bulk and rhizosphere soil samples were collected to assess the amendment-induced effects on four microbial lineages (bacteria, fungi, arbuscular mycorrhizal fungi [AMF], and nematodes) and their functions including Cd stabilization, nutrient cycling, and pathogen control. Compared with the control, both CMC application rates increased the pH and reduced labile Cd fraction in the bulk and rhizosphere soils. Although the total Cd concentrations in the soil were similar, the Cd accumulation in the grains was significantly reduced in treatments of soil amendments. It was observed that the application of CMC can significantly reduce the AMF diversity but increased the diversity of the other three communities. Moreover, the biodiversity within keystone modules (identified by co-occurrence network analysis) played key roles in driving soil multifunctionality. Specifically, key beneficial groups in module 2 such as Aggregicoccus (bacteria), Sordariomycetes (fungi), Glomus (AMF), and Bursaphelenchus (nematode) were strongly associated with soil multifunctionality. By co-culturing bacterial suspensions with the soybean root rot pathogen Fusarium solani in the in vitro assays, we experimentally validated that the application of CMC promoted the suppression of soil bacterial community on pathogens by inhibiting the mycelium growth and spore germination. Also, the bacterial community was more resistant to Cd stress in soils receiving CMC amendment. Our findings provide valuable theoretical references for enhancing soil functions and health via applying a soil amendment (CMC) during Cd-contaminated soil remediation. IMPORTANCE Restoration of microbiome-driven soil functions and health is of great importance during Cd-contaminated soil remediation via soil amendment. Soybean and its symbiotic mutualism can provide abundant nitrogen and phosphorus to relieve the nutrient deficiency of Cd-contaminated soil. This study provides a novel perspective on the potential role of applying a soil amendment (CMC) in enhancing the functions and health of Cd-contaminated soils. Our results showed the distinct differences in soil microbial community responding to amendment-induced changes in edaphic properties. The biodiversity within keystone modules had major contributions to the maintenance of the soil’s multifunctionality and health. Additionally, a higher CMC application rate showed more beneficial effects. Collectively, our results enhance our understanding about the effects of applying CMC, together with soybean rotation, to enhance and maintain soil functions and health during the field Cd stabilization process.
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spelling doaj.art-c1ca37c47ab64064a25a9bb074f385462023-06-29T13:00:40ZengAmerican Society for MicrobiologymSystems2379-50772023-06-018310.1128/msystems.01049-22Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendmentsZhongyi Cheng0Jiachun Shi1Yan He2Yuxuan Chen3Youjing Wang4Xueling Yang5Tianyu Wang6Laosheng Wu7Jianming Xu8Institute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaDepartment of Environmental Sciences, University of California , Riverside, California, USAInstitute of Soil and Water Resources and Environmental Science, College of Environmental and Resource Sciences, Zhejiang University , Hangzhou, ChinaABSTRACT The interactions between soil microbiomes at various trophic levels are essential for restoring soil functions. Legumes are considered as “pioneer crops” in degraded or contaminated soils because they can fix nitrogen through symbiotic relationships with rhizobacteria, which promotes soil fertility. However, little is known about the abilities of legumes to contribute to the health of soil contaminated with cadmium (Cd). In this research, we applied a soil amendment (commercial Mg–Ca–Si conditioner, CMC) at two rates (1,500 and 3,000 kg/ha) in a Cd-contaminated soybean field. Bulk and rhizosphere soil samples were collected to assess the amendment-induced effects on four microbial lineages (bacteria, fungi, arbuscular mycorrhizal fungi [AMF], and nematodes) and their functions including Cd stabilization, nutrient cycling, and pathogen control. Compared with the control, both CMC application rates increased the pH and reduced labile Cd fraction in the bulk and rhizosphere soils. Although the total Cd concentrations in the soil were similar, the Cd accumulation in the grains was significantly reduced in treatments of soil amendments. It was observed that the application of CMC can significantly reduce the AMF diversity but increased the diversity of the other three communities. Moreover, the biodiversity within keystone modules (identified by co-occurrence network analysis) played key roles in driving soil multifunctionality. Specifically, key beneficial groups in module 2 such as Aggregicoccus (bacteria), Sordariomycetes (fungi), Glomus (AMF), and Bursaphelenchus (nematode) were strongly associated with soil multifunctionality. By co-culturing bacterial suspensions with the soybean root rot pathogen Fusarium solani in the in vitro assays, we experimentally validated that the application of CMC promoted the suppression of soil bacterial community on pathogens by inhibiting the mycelium growth and spore germination. Also, the bacterial community was more resistant to Cd stress in soils receiving CMC amendment. Our findings provide valuable theoretical references for enhancing soil functions and health via applying a soil amendment (CMC) during Cd-contaminated soil remediation. IMPORTANCE Restoration of microbiome-driven soil functions and health is of great importance during Cd-contaminated soil remediation via soil amendment. Soybean and its symbiotic mutualism can provide abundant nitrogen and phosphorus to relieve the nutrient deficiency of Cd-contaminated soil. This study provides a novel perspective on the potential role of applying a soil amendment (CMC) in enhancing the functions and health of Cd-contaminated soils. Our results showed the distinct differences in soil microbial community responding to amendment-induced changes in edaphic properties. The biodiversity within keystone modules had major contributions to the maintenance of the soil’s multifunctionality and health. Additionally, a higher CMC application rate showed more beneficial effects. Collectively, our results enhance our understanding about the effects of applying CMC, together with soybean rotation, to enhance and maintain soil functions and health during the field Cd stabilization process.https://journals.asm.org/doi/10.1128/msystems.01049-22cadmium-contaminated soilsoil amendmentsoybeanmultitrophic community assemblymultifunctionalitydisease suppression
spellingShingle Zhongyi Cheng
Jiachun Shi
Yan He
Yuxuan Chen
Youjing Wang
Xueling Yang
Tianyu Wang
Laosheng Wu
Jianming Xu
Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments
mSystems
cadmium-contaminated soil
soil amendment
soybean
multitrophic community assembly
multifunctionality
disease suppression
title Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments
title_full Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments
title_fullStr Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments
title_full_unstemmed Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments
title_short Enhanced soil function and health by soybean root microbial communities during in situ remediation of Cd-contaminated soil with the application of soil amendments
title_sort enhanced soil function and health by soybean root microbial communities during in situ remediation of cd contaminated soil with the application of soil amendments
topic cadmium-contaminated soil
soil amendment
soybean
multitrophic community assembly
multifunctionality
disease suppression
url https://journals.asm.org/doi/10.1128/msystems.01049-22
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