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Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations

To maintain the beneficial effects of microbial inoculants on plants and soil, repeated inoculation represents a promising option. Until now, the impacts of one-off inoculation on the native microbiome have been explored, but it remains unclear how long and to what extent the periodic inoculations w...

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Autores principales: Wang, Zhikang, Chen, Ziyun, Kowalchuk, George A., Xu, Ziheng, Fu, Xiangxiang, Kuramae, Eiko E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8091015/
https://www.ncbi.nlm.nih.gov/pubmed/33637572
http://dx.doi.org/10.1128/AEM.00046-21
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author Wang, Zhikang
Chen, Ziyun
Kowalchuk, George A.
Xu, Ziheng
Fu, Xiangxiang
Kuramae, Eiko E.
author_facet Wang, Zhikang
Chen, Ziyun
Kowalchuk, George A.
Xu, Ziheng
Fu, Xiangxiang
Kuramae, Eiko E.
author_sort Wang, Zhikang
collection PubMed
description To maintain the beneficial effects of microbial inoculants on plants and soil, repeated inoculation represents a promising option. Until now, the impacts of one-off inoculation on the native microbiome have been explored, but it remains unclear how long and to what extent the periodic inoculations would affect the succession of the resident microbiome in bulk soil. Here, we examined the dynamic responses of plant growth, soil functions, and the resident bacterial community in the bulk soil to periodic inoculations of phosphate-solubilizing and N(2)-fixing bacteria alone or in combination. Compared to single-strain inoculation, coinoculation better stimulated plant growth and soil nutrients. However, the benefits from inoculants did not increase with repeated inoculations and were not maintained after transplantation to a different site. In response to microbial inoculants, three patterns of shifts in the bacterial composition were observed: fold increase, fold decrease, and resilience. The periodic inoculations impacted the succession course of resident bacterial communities in bulk soil, mainly driven by changes in soil pH and nitrate, resulting in the development of three main cluster types throughout the investigation. The single and mixed inoculants transiently modulated the variation in the resident community in association with soil pH and the C/N ratio, but finally, the community established and showed resilience to subsequent inoculations. Consequently, the necessity of repeated inoculations should be reconsidered, and while the different microbial inoculants showed distinct impacts on resident microbiome succession, the communities ultimately exhibited resilience. IMPORTANCE Introducing beneficial microbes to the plant-soil system is an environmentally friendly approach to improve the crop yield and soil environment. Numerous studies have attempted to reveal the impacts of inoculation on the rhizosphere microbiome. However, little is known about the effectiveness of periodic inoculations on soil functioning. In addition, the long-term impact of repeated inoculations on the native community remains unclear. Here, we track the succession traits of the resident microbiome in the bulk soil across a growing season and identify the taxon clusters that respond differently to periodic inoculation. Crucially, we compare the development of the resident community composition with and without inoculation, thus providing new insight into the interactions between resident microbes and intruders. Finally, we conclude that initial inoculation plays a more important role in influencing the whole system, and the native microbial community exhibits traits of resilience, but no resistance, to the subsequent inoculations.
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spelling pubmed-80910152021-10-13 Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations Wang, Zhikang Chen, Ziyun Kowalchuk, George A. Xu, Ziheng Fu, Xiangxiang Kuramae, Eiko E. Appl Environ Microbiol Microbial Ecology To maintain the beneficial effects of microbial inoculants on plants and soil, repeated inoculation represents a promising option. Until now, the impacts of one-off inoculation on the native microbiome have been explored, but it remains unclear how long and to what extent the periodic inoculations would affect the succession of the resident microbiome in bulk soil. Here, we examined the dynamic responses of plant growth, soil functions, and the resident bacterial community in the bulk soil to periodic inoculations of phosphate-solubilizing and N(2)-fixing bacteria alone or in combination. Compared to single-strain inoculation, coinoculation better stimulated plant growth and soil nutrients. However, the benefits from inoculants did not increase with repeated inoculations and were not maintained after transplantation to a different site. In response to microbial inoculants, three patterns of shifts in the bacterial composition were observed: fold increase, fold decrease, and resilience. The periodic inoculations impacted the succession course of resident bacterial communities in bulk soil, mainly driven by changes in soil pH and nitrate, resulting in the development of three main cluster types throughout the investigation. The single and mixed inoculants transiently modulated the variation in the resident community in association with soil pH and the C/N ratio, but finally, the community established and showed resilience to subsequent inoculations. Consequently, the necessity of repeated inoculations should be reconsidered, and while the different microbial inoculants showed distinct impacts on resident microbiome succession, the communities ultimately exhibited resilience. IMPORTANCE Introducing beneficial microbes to the plant-soil system is an environmentally friendly approach to improve the crop yield and soil environment. Numerous studies have attempted to reveal the impacts of inoculation on the rhizosphere microbiome. However, little is known about the effectiveness of periodic inoculations on soil functioning. In addition, the long-term impact of repeated inoculations on the native community remains unclear. Here, we track the succession traits of the resident microbiome in the bulk soil across a growing season and identify the taxon clusters that respond differently to periodic inoculation. Crucially, we compare the development of the resident community composition with and without inoculation, thus providing new insight into the interactions between resident microbes and intruders. Finally, we conclude that initial inoculation plays a more important role in influencing the whole system, and the native microbial community exhibits traits of resilience, but no resistance, to the subsequent inoculations. American Society for Microbiology 2021-04-13 /pmc/articles/PMC8091015/ /pubmed/33637572 http://dx.doi.org/10.1128/AEM.00046-21 Text en Copyright © 2021 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Microbial Ecology
Wang, Zhikang
Chen, Ziyun
Kowalchuk, George A.
Xu, Ziheng
Fu, Xiangxiang
Kuramae, Eiko E.
Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations
title Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations
title_full Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations
title_fullStr Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations
title_full_unstemmed Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations
title_short Succession of the Resident Soil Microbial Community in Response to Periodic Inoculations
title_sort succession of the resident soil microbial community in response to periodic inoculations
topic Microbial Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8091015/
https://www.ncbi.nlm.nih.gov/pubmed/33637572
http://dx.doi.org/10.1128/AEM.00046-21
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