Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes

ABSTRACT It is a central ecological goal to explore the effects of global change factors on soil microbial communities. The vast functional gene repertoire of soil microbial communities is composed of both core and accessory genes, which may be governed by distinct drivers. This intuitive hypothesis...

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Autores principales: Ximei Zhang, Eric R. Johnston, Yaosheng Wang, Qiang Yu, Dashuan Tian, Zhiping Wang, Yanqing Zhang, Daozhi Gong, Chun Luo, Wei Liu, Junjie Yang, Xingguo Han
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:b1ca5cd7f3ea46ada5033bb7b3e07ef92021-12-02T18:39:15ZDistinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes10.1128/mSystems.00374-192379-5077https://doaj.org/article/b1ca5cd7f3ea46ada5033bb7b3e07ef92019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00374-19https://doaj.org/toc/2379-5077ABSTRACT It is a central ecological goal to explore the effects of global change factors on soil microbial communities. The vast functional gene repertoire of soil microbial communities is composed of both core and accessory genes, which may be governed by distinct drivers. This intuitive hypothesis, however, remains largely unexplored. We conducted a 5-year nitrogen and water addition experiment in the Eurasian steppe and quantified microbial gene diversity via shotgun metagenomics. Nitrogen addition led to an 11-fold increase in the abundance (based on quantitative PCR [qPCR]) of ammonia-oxidizing bacteria, which have mainly core community genes and few accessory community genes. Thus, nitrogen addition substantially increased the relative abundance of many core genes at the whole-community level. Water addition stimulated both plant diversity and microbial respiration; however, increased carbon/energy resources from plants did not counteract increased respiration, so soil carbon/energy resources became more limited. Thus, water addition selected for microorganisms with genes responsible for degrading recalcitrant soil organic matter. Accordingly, many other microorganisms without these genes (but likely with other accessory community genes due to relatively stable average microbial genome size) were selected against, leading to the decrease in the diversity of accessory community genes. In summary, nitrogen addition primarily affected core community genes through nitrogen-cycling processes, and water addition primarily regulated accessory community genes through carbon-cycling processes. Although both gene components may significantly respond as the intensity of nitrogen/water addition increases, our results demonstrated how these common global change factors distinctly impact each component. IMPORTANCE Our results demonstrated increased ecosystem nitrogen and water content as the primary drivers of the core and accessory components of soil microbial community functional diversity, respectively. Our findings suggested that more attention should be paid to certain components of community functional diversity under specific global change conditions. Our findings also indicated that microbial communities have adapted to nitrogen addition by strengthening the function of ammonia oxidization to deplete the excess nitrogen, thus maintaining ecosystem homeostasis. Because community gene richness is primarily determined by the presence/absence of accessory community genes, our findings further implied that strategies such as maintaining the amount of soil organic matter could be adopted to effectively improve the functional gene diversity of soil microbial communities subject to global change factors.Ximei ZhangEric R. JohnstonYaosheng WangQiang YuDashuan TianZhiping WangYanqing ZhangDaozhi GongChun LuoWei LiuJunjie YangXingguo HanAmerican Society for Microbiologyarticleaccessory community genecore community genegrasslandincreased precipitationmicrobial diversitynitrogen depositionMicrobiologyQR1-502ENmSystems, Vol 4, Iss 5 (2019)
institution DOAJ
collection DOAJ
language EN
topic accessory community gene
core community gene
grassland
increased precipitation
microbial diversity
nitrogen deposition
Microbiology
QR1-502
spellingShingle accessory community gene
core community gene
grassland
increased precipitation
microbial diversity
nitrogen deposition
Microbiology
QR1-502
Ximei Zhang
Eric R. Johnston
Yaosheng Wang
Qiang Yu
Dashuan Tian
Zhiping Wang
Yanqing Zhang
Daozhi Gong
Chun Luo
Wei Liu
Junjie Yang
Xingguo Han
Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
description ABSTRACT It is a central ecological goal to explore the effects of global change factors on soil microbial communities. The vast functional gene repertoire of soil microbial communities is composed of both core and accessory genes, which may be governed by distinct drivers. This intuitive hypothesis, however, remains largely unexplored. We conducted a 5-year nitrogen and water addition experiment in the Eurasian steppe and quantified microbial gene diversity via shotgun metagenomics. Nitrogen addition led to an 11-fold increase in the abundance (based on quantitative PCR [qPCR]) of ammonia-oxidizing bacteria, which have mainly core community genes and few accessory community genes. Thus, nitrogen addition substantially increased the relative abundance of many core genes at the whole-community level. Water addition stimulated both plant diversity and microbial respiration; however, increased carbon/energy resources from plants did not counteract increased respiration, so soil carbon/energy resources became more limited. Thus, water addition selected for microorganisms with genes responsible for degrading recalcitrant soil organic matter. Accordingly, many other microorganisms without these genes (but likely with other accessory community genes due to relatively stable average microbial genome size) were selected against, leading to the decrease in the diversity of accessory community genes. In summary, nitrogen addition primarily affected core community genes through nitrogen-cycling processes, and water addition primarily regulated accessory community genes through carbon-cycling processes. Although both gene components may significantly respond as the intensity of nitrogen/water addition increases, our results demonstrated how these common global change factors distinctly impact each component. IMPORTANCE Our results demonstrated increased ecosystem nitrogen and water content as the primary drivers of the core and accessory components of soil microbial community functional diversity, respectively. Our findings suggested that more attention should be paid to certain components of community functional diversity under specific global change conditions. Our findings also indicated that microbial communities have adapted to nitrogen addition by strengthening the function of ammonia oxidization to deplete the excess nitrogen, thus maintaining ecosystem homeostasis. Because community gene richness is primarily determined by the presence/absence of accessory community genes, our findings further implied that strategies such as maintaining the amount of soil organic matter could be adopted to effectively improve the functional gene diversity of soil microbial communities subject to global change factors.
format article
author Ximei Zhang
Eric R. Johnston
Yaosheng Wang
Qiang Yu
Dashuan Tian
Zhiping Wang
Yanqing Zhang
Daozhi Gong
Chun Luo
Wei Liu
Junjie Yang
Xingguo Han
author_facet Ximei Zhang
Eric R. Johnston
Yaosheng Wang
Qiang Yu
Dashuan Tian
Zhiping Wang
Yanqing Zhang
Daozhi Gong
Chun Luo
Wei Liu
Junjie Yang
Xingguo Han
author_sort Ximei Zhang
title Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
title_short Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
title_full Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
title_fullStr Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
title_full_unstemmed Distinct Drivers of Core and Accessory Components of Soil Microbial Community Functional Diversity under Environmental Changes
title_sort distinct drivers of core and accessory components of soil microbial community functional diversity under environmental changes
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/b1ca5cd7f3ea46ada5033bb7b3e07ef9
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