Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation

Casuarina equisetifolia (C. equisetifolia) is an economically important forest tree species, often cultivated in continuous monoculture as a coastal protection forest. Continuous planting has gradually affected growth and severely restricted the sustainable development of the C. equisetifolia indust...

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Main Authors: Yuhua Wang, Shaoxiong Lin, Jianjuan Li, Xiaoli Jia, Mingyue Hu, Yuhong Cai, Pengyuan Cheng, Mingzhe Li, Yiling Chen, Wenxiong Lin, Haibin Wang, Zeyan Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1324184/full
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author Yuhua Wang
Yuhua Wang
Shaoxiong Lin
Jianjuan Li
Xiaoli Jia
Xiaoli Jia
Mingyue Hu
Mingyue Hu
Yuhong Cai
Yuhong Cai
Pengyuan Cheng
Mingzhe Li
Yiling Chen
Wenxiong Lin
Wenxiong Lin
Haibin Wang
Haibin Wang
Zeyan Wu
Zeyan Wu
author_facet Yuhua Wang
Yuhua Wang
Shaoxiong Lin
Jianjuan Li
Xiaoli Jia
Xiaoli Jia
Mingyue Hu
Mingyue Hu
Yuhong Cai
Yuhong Cai
Pengyuan Cheng
Mingzhe Li
Yiling Chen
Wenxiong Lin
Wenxiong Lin
Haibin Wang
Haibin Wang
Zeyan Wu
Zeyan Wu
author_sort Yuhua Wang
collection DOAJ
description Casuarina equisetifolia (C. equisetifolia) is an economically important forest tree species, often cultivated in continuous monoculture as a coastal protection forest. Continuous planting has gradually affected growth and severely restricted the sustainable development of the C. equisetifolia industry. In this study, we analyzed the effects of continuous planting on C. equisetifolia growth and explored the rhizosphere soil microecological mechanism from a metagenomic perspective. The results showed that continuous planting resulted in dwarfing, shorter root length, and reduced C. equisetifolia seedling root system. Metagenomics analysis showed that 10 key characteristic microorganisms, mainly Actinoallomurus, Actinomadura, and Mycobacterium, were responsible for continuously planted C. equisetifolia trees. Quantitative analysis showed that the number of microorganisms in these three genera decreased significantly with the increase of continuous planting. Gene function analysis showed that continuous planting led to the weakening of the environmental information processing-signal transduction ability of soil characteristic microorganisms, and the decrease of C. equisetifolia trees against stress. Reduced capacity for metabolism, genetic information processing-replication and repair resulted in reduced microbial propagation and reduced microbial quantity in the rhizosphere soil of C. equisetifolia trees. Secondly, amino acid metabolism, carbohydrate metabolism, glycan biosynthesis and metabolism, lipid metabolism, metabolism of cofactors and vitamins were all significantly reduced, resulting in a decrease in the ability of the soil to synthesize and metabolize carbon and nitrogen. These reduced capacities further led to reduced soil microbial quantity, microbial carbon and nitrogen, microbial respiration intensity, reduced soil enzyme nutrient cycling and resistance-related enzyme activities, a significant reduction in available nutrient content of rhizosphere soils, a reduction in the ion exchange capacity, and an impediment to C. equisetifolia growth. This study provides an important basis for the management of continuously planted C. equisetifolia plantations.
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spelling doaj.art-ab41cc1cda6444be8dda8ef26c4f23882023-12-06T08:36:39ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-12-011410.3389/fpls.2023.13241841324184Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformationYuhua Wang0Yuhua Wang1Shaoxiong Lin2Jianjuan Li3Xiaoli Jia4Xiaoli Jia5Mingyue Hu6Mingyue Hu7Yuhong Cai8Yuhong Cai9Pengyuan Cheng10Mingzhe Li11Yiling Chen12Wenxiong Lin13Wenxiong Lin14Haibin Wang15Haibin Wang16Zeyan Wu17Zeyan Wu18College of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Life Science, Longyan University, Longyan, ChinaEditorial Department, Fujian Academy of Forestry Survey and Planning, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Tea and Food, Wuyi University, Wuyishan, ChinaCollege of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Life Science, Longyan University, Longyan, ChinaCollege of Life Science, Longyan University, Longyan, ChinaCollege of Life Science, Longyan University, Longyan, ChinaCollege of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Tea and Food, Wuyi University, Wuyishan, ChinaCollege of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Provincial Key Laboratory of Agroecological Processing and Safety Monitoring, College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaCasuarina equisetifolia (C. equisetifolia) is an economically important forest tree species, often cultivated in continuous monoculture as a coastal protection forest. Continuous planting has gradually affected growth and severely restricted the sustainable development of the C. equisetifolia industry. In this study, we analyzed the effects of continuous planting on C. equisetifolia growth and explored the rhizosphere soil microecological mechanism from a metagenomic perspective. The results showed that continuous planting resulted in dwarfing, shorter root length, and reduced C. equisetifolia seedling root system. Metagenomics analysis showed that 10 key characteristic microorganisms, mainly Actinoallomurus, Actinomadura, and Mycobacterium, were responsible for continuously planted C. equisetifolia trees. Quantitative analysis showed that the number of microorganisms in these three genera decreased significantly with the increase of continuous planting. Gene function analysis showed that continuous planting led to the weakening of the environmental information processing-signal transduction ability of soil characteristic microorganisms, and the decrease of C. equisetifolia trees against stress. Reduced capacity for metabolism, genetic information processing-replication and repair resulted in reduced microbial propagation and reduced microbial quantity in the rhizosphere soil of C. equisetifolia trees. Secondly, amino acid metabolism, carbohydrate metabolism, glycan biosynthesis and metabolism, lipid metabolism, metabolism of cofactors and vitamins were all significantly reduced, resulting in a decrease in the ability of the soil to synthesize and metabolize carbon and nitrogen. These reduced capacities further led to reduced soil microbial quantity, microbial carbon and nitrogen, microbial respiration intensity, reduced soil enzyme nutrient cycling and resistance-related enzyme activities, a significant reduction in available nutrient content of rhizosphere soils, a reduction in the ion exchange capacity, and an impediment to C. equisetifolia growth. This study provides an important basis for the management of continuously planted C. equisetifolia plantations.https://www.frontiersin.org/articles/10.3389/fpls.2023.1324184/fullC. equisetifoliacontinuous plantingmetagenomenutrient transformationsoil enzymesgene function
spellingShingle Yuhua Wang
Yuhua Wang
Shaoxiong Lin
Jianjuan Li
Xiaoli Jia
Xiaoli Jia
Mingyue Hu
Mingyue Hu
Yuhong Cai
Yuhong Cai
Pengyuan Cheng
Mingzhe Li
Yiling Chen
Wenxiong Lin
Wenxiong Lin
Haibin Wang
Haibin Wang
Zeyan Wu
Zeyan Wu
Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
Frontiers in Plant Science
C. equisetifolia
continuous planting
metagenome
nutrient transformation
soil enzymes
gene function
title Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
title_full Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
title_fullStr Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
title_full_unstemmed Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
title_short Metagenomics-based exploration of key soil microorganisms contributing to continuously planted Casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
title_sort metagenomics based exploration of key soil microorganisms contributing to continuously planted casuarina equisetifolia growth inhibition and their interactions with soil nutrient transformation
topic C. equisetifolia
continuous planting
metagenome
nutrient transformation
soil enzymes
gene function
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1324184/full
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