Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress
Abstract Background The prokaryotic antiviral defense systems are crucial for mediating prokaryote-virus interactions that influence microbiome functioning and evolutionary dynamics. Despite the prevalence and significance of prokaryotic antiviral defense systems, their responses to abiotic stress a...
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BMC
2025-01-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-025-02030-z |
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| author | Dan Huang Jingqiu Liao Jose Luis Balcazar Mao Ye Ruonan Wu Dongsheng Wang Pedro J. J. Alvarez Pingfeng Yu |
| author_facet | Dan Huang Jingqiu Liao Jose Luis Balcazar Mao Ye Ruonan Wu Dongsheng Wang Pedro J. J. Alvarez Pingfeng Yu |
| author_sort | Dan Huang |
| collection | DOAJ |
| description | Abstract Background The prokaryotic antiviral defense systems are crucial for mediating prokaryote-virus interactions that influence microbiome functioning and evolutionary dynamics. Despite the prevalence and significance of prokaryotic antiviral defense systems, their responses to abiotic stress and ecological consequences remain poorly understood in soil ecosystems. We established microcosm systems with varying concentrations of hexavalent chromium (Cr(VI)) to investigate the adaptive modifications of prokaryotic antiviral defense systems under abiotic stress. Results Utilizing hybrid metagenomic assembly with long-read and short-read sequencing, we discovered that antiviral defense systems were more diverse and prevalent in heavily polluted soils, which was corroborated by meta-analyses of public datasets from various heavy metal-contaminated sites. As the Cr(VI) concentration increased, prokaryotes with defense systems favoring prokaryote-virus mutualism gradually supplanted those with defense systems incurring high adaptive costs. Additionally, as Cr(VI) concentrations increased, enriched antiviral defense systems exhibited synchronization with microbial heavy metal resistance genes. Furthermore, the proportion of antiviral defense systems carried by mobile genetic elements (MGEs), including plasmids and viruses, increased by approximately 43% and 39%, respectively, with rising Cr concentrations. This trend is conducive to strengthening the dissemination and sharing of defense resources within microbial communities. Conclusions Overall, our study reveals the adaptive modification of prokaryotic antiviral defense systems in soil ecosystems under abiotic stress, as well as their positive contributions to establishing prokaryote-virus mutualism and the evolution of microbial heavy metal resistance. These findings advance our understanding of microbial adaptation in stressful environments and may inspire novel approaches for microbiome manipulation and bioremediation. Video Abstract |
| format | Article |
| id | doaj-art-2bda8976c0bd4d4ea68a5d1935cbb4a5 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj-art-2bda8976c0bd4d4ea68a5d1935cbb4a52025-02-02T12:33:55ZengBMCMicrobiome2049-26182025-01-0113111610.1186/s40168-025-02030-zAdaptive modification of antiviral defense systems in microbial community under Cr-induced stressDan Huang0Jingqiu Liao1Jose Luis Balcazar2Mao Ye3Ruonan Wu4Dongsheng Wang5Pedro J. J. Alvarez6Pingfeng Yu7College of Environmental and Resource Sciences, Zhejiang UniversityDepartment of Civil and Environmental Engineering, Virginia TechCatalan Institute for Water Research (ICRA-CERCA)Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of SciencesEarth and Biological Sciences Directorate, Pacific Northwest National LabCollege of Environmental and Resource Sciences, Zhejiang UniversityDepartment of Civil and Environmental Engineering, Rice UniversityCollege of Environmental and Resource Sciences, Zhejiang UniversityAbstract Background The prokaryotic antiviral defense systems are crucial for mediating prokaryote-virus interactions that influence microbiome functioning and evolutionary dynamics. Despite the prevalence and significance of prokaryotic antiviral defense systems, their responses to abiotic stress and ecological consequences remain poorly understood in soil ecosystems. We established microcosm systems with varying concentrations of hexavalent chromium (Cr(VI)) to investigate the adaptive modifications of prokaryotic antiviral defense systems under abiotic stress. Results Utilizing hybrid metagenomic assembly with long-read and short-read sequencing, we discovered that antiviral defense systems were more diverse and prevalent in heavily polluted soils, which was corroborated by meta-analyses of public datasets from various heavy metal-contaminated sites. As the Cr(VI) concentration increased, prokaryotes with defense systems favoring prokaryote-virus mutualism gradually supplanted those with defense systems incurring high adaptive costs. Additionally, as Cr(VI) concentrations increased, enriched antiviral defense systems exhibited synchronization with microbial heavy metal resistance genes. Furthermore, the proportion of antiviral defense systems carried by mobile genetic elements (MGEs), including plasmids and viruses, increased by approximately 43% and 39%, respectively, with rising Cr concentrations. This trend is conducive to strengthening the dissemination and sharing of defense resources within microbial communities. Conclusions Overall, our study reveals the adaptive modification of prokaryotic antiviral defense systems in soil ecosystems under abiotic stress, as well as their positive contributions to establishing prokaryote-virus mutualism and the evolution of microbial heavy metal resistance. These findings advance our understanding of microbial adaptation in stressful environments and may inspire novel approaches for microbiome manipulation and bioremediation. Video Abstracthttps://doi.org/10.1186/s40168-025-02030-zAntiviral defense systemProkaryote-virus interactionsHeavy metal resistanceMobile genetic elementsHybrid metagenomics |
| spellingShingle | Dan Huang Jingqiu Liao Jose Luis Balcazar Mao Ye Ruonan Wu Dongsheng Wang Pedro J. J. Alvarez Pingfeng Yu Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress Microbiome Antiviral defense system Prokaryote-virus interactions Heavy metal resistance Mobile genetic elements Hybrid metagenomics |
| title | Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress |
| title_full | Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress |
| title_fullStr | Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress |
| title_full_unstemmed | Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress |
| title_short | Adaptive modification of antiviral defense systems in microbial community under Cr-induced stress |
| title_sort | adaptive modification of antiviral defense systems in microbial community under cr induced stress |
| topic | Antiviral defense system Prokaryote-virus interactions Heavy metal resistance Mobile genetic elements Hybrid metagenomics |
| url | https://doi.org/10.1186/s40168-025-02030-z |
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