Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants

Abstract Background The ubiquitous gut microbiotas acquired from the environment contribute to host health. The gut microbiotas of soil invertebrates are gradually assembled from the microecological region of the soil ecosystem which they inhabit, but little is known about their characteristics when...

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Main Authors: Qi Zhang, Zhenyan Zhang, Tao Lu, Yitian Yu, Josep Penuelas, Yong-Guan Zhu, Haifeng Qian
Format: Article
Language:English
Published: BMC 2021-09-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-021-01150-6
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author Qi Zhang
Zhenyan Zhang
Tao Lu
Yitian Yu
Josep Penuelas
Yong-Guan Zhu
Haifeng Qian
author_facet Qi Zhang
Zhenyan Zhang
Tao Lu
Yitian Yu
Josep Penuelas
Yong-Guan Zhu
Haifeng Qian
author_sort Qi Zhang
collection DOAJ
description Abstract Background The ubiquitous gut microbiotas acquired from the environment contribute to host health. The gut microbiotas of soil invertebrates are gradually assembled from the microecological region of the soil ecosystem which they inhabit, but little is known about their characteristics when the hosts are under environmental stress. The rapid development of high-throughput DNA sequencing in the last decade has provided unprecedented insights and opportunities to characterize the gut microbiotas of soil invertebrates. Here, we characterized the core, transient, and rare bacterial taxa in the guts of soil invertebrates using the core index (CI) and developed a new theory of global microbial diversity of soil ecological microregions. Results We found that the Gammaproteobacteria could respond indiscriminately to the exposure to environmental concentrations of soil pollutants and were closely associated with the physiology and function of the host. Meanwhile, machine-learning models based on metadata calculated that Gammaproteobacteria were the core bacteria with the highest colonization potential in the gut, and further identified that they were the best indicator taxon of the response to environmental concentrations of soil pollution. Gammaproteobacteria also closely correlated with the abundance of antibiotic resistance genes. Conclusions Our results determined that Gammaproteobacteria were an indicator taxon in the guts of the soil invertebrates that responded to environmental concentrations of soil pollutants, thus providing an effective theoretical basis for subsequent assessments of soil ecological risk. The results of the physiological and biochemical analyses of the host and the microbial-community functions, and the antibiotic resistance of Gammaproteobacteria, provide new insights for evaluating global soil ecological health. Video abstract
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spelling doaj.art-11d8951e608e48e8be50206abea63f9b2022-12-21T22:37:09ZengBMCMicrobiome2049-26182021-09-019111710.1186/s40168-021-01150-6Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutantsQi Zhang0Zhenyan Zhang1Tao Lu2Yitian Yu3Josep Penuelas4Yong-Guan Zhu5Haifeng Qian6College of Environment, Zhejiang University of TechnologyCollege of Environment, Zhejiang University of TechnologyCollege of Environment, Zhejiang University of TechnologyCollege of Environment, Zhejiang University of TechnologyGlobal Ecology Unit CREAF-CSIC-UAB, CSICKey Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of SciencesCollege of Environment, Zhejiang University of TechnologyAbstract Background The ubiquitous gut microbiotas acquired from the environment contribute to host health. The gut microbiotas of soil invertebrates are gradually assembled from the microecological region of the soil ecosystem which they inhabit, but little is known about their characteristics when the hosts are under environmental stress. The rapid development of high-throughput DNA sequencing in the last decade has provided unprecedented insights and opportunities to characterize the gut microbiotas of soil invertebrates. Here, we characterized the core, transient, and rare bacterial taxa in the guts of soil invertebrates using the core index (CI) and developed a new theory of global microbial diversity of soil ecological microregions. Results We found that the Gammaproteobacteria could respond indiscriminately to the exposure to environmental concentrations of soil pollutants and were closely associated with the physiology and function of the host. Meanwhile, machine-learning models based on metadata calculated that Gammaproteobacteria were the core bacteria with the highest colonization potential in the gut, and further identified that they were the best indicator taxon of the response to environmental concentrations of soil pollution. Gammaproteobacteria also closely correlated with the abundance of antibiotic resistance genes. Conclusions Our results determined that Gammaproteobacteria were an indicator taxon in the guts of the soil invertebrates that responded to environmental concentrations of soil pollutants, thus providing an effective theoretical basis for subsequent assessments of soil ecological risk. The results of the physiological and biochemical analyses of the host and the microbial-community functions, and the antibiotic resistance of Gammaproteobacteria, provide new insights for evaluating global soil ecological health. Video abstracthttps://doi.org/10.1186/s40168-021-01150-6Gut microbiotaPesticideIndicator taxaMachine learningSoil invertebrateAntibiotic resistance genes
spellingShingle Qi Zhang
Zhenyan Zhang
Tao Lu
Yitian Yu
Josep Penuelas
Yong-Guan Zhu
Haifeng Qian
Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants
Microbiome
Gut microbiota
Pesticide
Indicator taxa
Machine learning
Soil invertebrate
Antibiotic resistance genes
title Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants
title_full Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants
title_fullStr Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants
title_full_unstemmed Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants
title_short Gammaproteobacteria, a core taxon in the guts of soil fauna, are potential responders to environmental concentrations of soil pollutants
title_sort gammaproteobacteria a core taxon in the guts of soil fauna are potential responders to environmental concentrations of soil pollutants
topic Gut microbiota
Pesticide
Indicator taxa
Machine learning
Soil invertebrate
Antibiotic resistance genes
url https://doi.org/10.1186/s40168-021-01150-6
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