Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts

Abstract Background Viral-encoded auxiliary metabolic genes (AMGs) are important toolkits for modulating their hosts’ metabolisms and the microbial-driven biogeochemical cycles. Although the functions of AMGs have been extensively reported in numerous environments, we still know little about the dri...

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Main Authors: Xiao-Qing Luo, Pandeng Wang, Jia-Ling Li, Manzoor Ahmad, Li Duan, Ling-Zi Yin, Qi-Qi Deng, Bao-Zhu Fang, Shan-Hui Li, Wen-Jun Li
Format: Article
Language:English
Published: BMC 2022-11-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-022-01384-y
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author Xiao-Qing Luo
Pandeng Wang
Jia-Ling Li
Manzoor Ahmad
Li Duan
Ling-Zi Yin
Qi-Qi Deng
Bao-Zhu Fang
Shan-Hui Li
Wen-Jun Li
author_facet Xiao-Qing Luo
Pandeng Wang
Jia-Ling Li
Manzoor Ahmad
Li Duan
Ling-Zi Yin
Qi-Qi Deng
Bao-Zhu Fang
Shan-Hui Li
Wen-Jun Li
author_sort Xiao-Qing Luo
collection DOAJ
description Abstract Background Viral-encoded auxiliary metabolic genes (AMGs) are important toolkits for modulating their hosts’ metabolisms and the microbial-driven biogeochemical cycles. Although the functions of AMGs have been extensively reported in numerous environments, we still know little about the drivers that shape the viral community-wide AMG compositions in natural ecosystems. Exploring the drivers of viral community-wide AMG compositions is critical for a deeper understanding of the complex interplays among viruses, hosts, and the environments. Results Here, we investigated the impact of viral lifestyles (i.e., lytic and lysogenic), habitats (i.e., water, particle, and sediment), and prokaryotic hosts on viral AMG profiles by utilizing metagenomic and metatranscriptomic techniques. We found that viral lifestyles were the most important drivers, followed by habitats and host identities. Specifically, irrespective of what habitats viruses came from, lytic viruses exhibited greater AMG diversity and tended to encode AMGs for chaperone biosynthesis, signaling proteins, and lipid metabolism, which could boost progeny reproduction, whereas temperate viruses were apt to encode AMGs for host survivability. Moreover, the lytic and temperate viral communities tended to mediate the microbial-driven biogeochemical cycles, especially nitrogen metabolism, in different manners via AMGs. When focusing on each lifestyle, we further found clear dissimilarity in AMG compositions between water and sediment, as well the divergent AMGs encoded by viruses infecting different host orders. Conclusions Overall, our study provides a first systematic characterization of the drivers of viral community-wide AMG compositions and further expands our knowledge of the distinct interactions of lytic and temperate viruses with their prokaryotic hosts from an AMG perspective, which is critical for understanding virus-host-environment interactions in natural conditions. Video Abstract
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spelling doaj.art-e5bb05deec124ba8b38817692711a8902022-12-22T03:58:04ZengBMCMicrobiome2049-26182022-11-0110111810.1186/s40168-022-01384-yViral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hostsXiao-Qing Luo0Pandeng Wang1Jia-Ling Li2Manzoor Ahmad3Li Duan4Ling-Zi Yin5Qi-Qi Deng6Bao-Zhu Fang7Shan-Hui Li8Wen-Jun Li9State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of SciencesState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityState Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-Sen UniversityAbstract Background Viral-encoded auxiliary metabolic genes (AMGs) are important toolkits for modulating their hosts’ metabolisms and the microbial-driven biogeochemical cycles. Although the functions of AMGs have been extensively reported in numerous environments, we still know little about the drivers that shape the viral community-wide AMG compositions in natural ecosystems. Exploring the drivers of viral community-wide AMG compositions is critical for a deeper understanding of the complex interplays among viruses, hosts, and the environments. Results Here, we investigated the impact of viral lifestyles (i.e., lytic and lysogenic), habitats (i.e., water, particle, and sediment), and prokaryotic hosts on viral AMG profiles by utilizing metagenomic and metatranscriptomic techniques. We found that viral lifestyles were the most important drivers, followed by habitats and host identities. Specifically, irrespective of what habitats viruses came from, lytic viruses exhibited greater AMG diversity and tended to encode AMGs for chaperone biosynthesis, signaling proteins, and lipid metabolism, which could boost progeny reproduction, whereas temperate viruses were apt to encode AMGs for host survivability. Moreover, the lytic and temperate viral communities tended to mediate the microbial-driven biogeochemical cycles, especially nitrogen metabolism, in different manners via AMGs. When focusing on each lifestyle, we further found clear dissimilarity in AMG compositions between water and sediment, as well the divergent AMGs encoded by viruses infecting different host orders. Conclusions Overall, our study provides a first systematic characterization of the drivers of viral community-wide AMG compositions and further expands our knowledge of the distinct interactions of lytic and temperate viruses with their prokaryotic hosts from an AMG perspective, which is critical for understanding virus-host-environment interactions in natural conditions. Video Abstracthttps://doi.org/10.1186/s40168-022-01384-yAuxiliary metabolic genes (AMGs)Viral lifestylesMetagenomes and metatranscriptomesBiogeochemical cycles
spellingShingle Xiao-Qing Luo
Pandeng Wang
Jia-Ling Li
Manzoor Ahmad
Li Duan
Ling-Zi Yin
Qi-Qi Deng
Bao-Zhu Fang
Shan-Hui Li
Wen-Jun Li
Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts
Microbiome
Auxiliary metabolic genes (AMGs)
Viral lifestyles
Metagenomes and metatranscriptomes
Biogeochemical cycles
title Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts
title_full Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts
title_fullStr Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts
title_full_unstemmed Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts
title_short Viral community-wide auxiliary metabolic genes differ by lifestyles, habitats, and hosts
title_sort viral community wide auxiliary metabolic genes differ by lifestyles habitats and hosts
topic Auxiliary metabolic genes (AMGs)
Viral lifestyles
Metagenomes and metatranscriptomes
Biogeochemical cycles
url https://doi.org/10.1186/s40168-022-01384-y
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