Huang Dan, Liao Jingqiu, Balcazar Jose Luis, Ye Mao, Wu Ruonan, Wang Dongsheng, Alvarez Pedro J J, Yu Pingfeng
College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, 310058, China.
Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA, 24060, USA.
Microbiome. 2025 Jan 31;13(1):34. doi: 10.1186/s40168-025-02030-z.
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.
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.
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.
原核生物抗病毒防御系统对于介导影响微生物群落功能和进化动态的原核生物 - 病毒相互作用至关重要。尽管原核生物抗病毒防御系统普遍存在且具有重要意义，但在土壤生态系统中，它们对非生物胁迫的反应及其生态后果仍知之甚少。我们建立了含有不同浓度六价铬（Cr(VI)）的微观系统，以研究非生物胁迫下原核生物抗病毒防御系统的适应性变化。
利用长读长和短读长测序的混合宏基因组组装，我们发现抗病毒防御系统在重度污染土壤中更加多样且普遍，这一点通过对来自各种重金属污染场地的公共数据集的荟萃分析得到了证实。随着Cr(VI)浓度的增加，具有有利于原核生物 - 病毒共生的防御系统的原核生物逐渐取代了那些具有高适应成本防御系统的原核生物。此外，随着Cr(VI)浓度的增加，富集的抗病毒防御系统与微生物重金属抗性基因表现出同步性。此外，随着Cr浓度的升高，包括质粒和病毒在内的移动遗传元件（MGEs）携带的抗病毒防御系统的比例分别增加了约43%和39%。这种趋势有利于加强微生物群落内防御资源的传播和共享。
总体而言，我们的研究揭示了非生物胁迫下土壤生态系统中原核生物抗病毒防御系统的适应性变化，以及它们对建立原核生物 - 病毒共生和微生物重金属抗性进化的积极贡献。这些发现推进了我们对压力环境下微生物适应性的理解，并可能激发微生物群落操纵和生物修复的新方法。视频摘要。
