Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits
Abstract Background Prokaryote-virus interactions play key roles in driving biogeochemical cycles. However, little is known about the drivers shaping their interaction network structures, especially from the host features. Here, we compiled 7656 species-level genomes in 39 prokaryotic phyla across e...
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| Format: | Article |
| Language: | English |
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BMC
2022-06-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-022-01288-x |
| _version_ | 1818555350411902976 |
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| author | Zhenghua Liu Qingyun Yan Chengying Jiang Juan Li Huahua Jian Lu Fan Rui Zhang Xiang Xiao Delong Meng Xueduan Liu Jianjun Wang Huaqun Yin |
| author_facet | Zhenghua Liu Qingyun Yan Chengying Jiang Juan Li Huahua Jian Lu Fan Rui Zhang Xiang Xiao Delong Meng Xueduan Liu Jianjun Wang Huaqun Yin |
| author_sort | Zhenghua Liu |
| collection | DOAJ |
| description | Abstract Background Prokaryote-virus interactions play key roles in driving biogeochemical cycles. However, little is known about the drivers shaping their interaction network structures, especially from the host features. Here, we compiled 7656 species-level genomes in 39 prokaryotic phyla across environments globally and explored how their interaction specialization is constrained by host life history traits, such as growth rate. Results We first reported that host growth rate indicated by the reverse of minimal doubling time was negatively related to interaction specialization for host in host-provirus network across various ecosystems and taxonomy groups. Such a negative linear growth rate-specialization relationship (GrSR) was dependent on host optimal growth temperature (OGT), and stronger toward the two gradient ends of OGT. For instance, prokaryotic species with an OGT ≥ 40 °C showed a stronger GrSR (Pearson’s r = −0.525, P < 0.001). Significant GrSRs were observed with the presences of host genes in promoting the infection cycle at stages of adsorption, establishment, and viral release, but nonsignificant with the presence of immune systems, such as restriction-modification systems and CRISPR-Cas systems. Moreover, GrSR strength was increased with the presence of temperature-dependent lytic switches, which was also confirmed by mathematical modeling. Conclusions Together, our results advance our understanding of the interactions between prokaryotes and proviruses and highlight the importance of host growth rate in interaction specialization during lysogenization. Video Abstract |
| first_indexed | 2024-12-12T09:52:13Z |
| format | Article |
| id | doaj.art-9ed9b7a6205848d2853de0dbb553348e |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-12T09:52:13Z |
| publishDate | 2022-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-9ed9b7a6205848d2853de0dbb553348e2022-12-22T00:28:14ZengBMCMicrobiome2049-26182022-06-0110111310.1186/s40168-022-01288-xGrowth rate determines prokaryote-provirus network modulated by temperature and host genetic traitsZhenghua Liu0Qingyun Yan1Chengying Jiang2Juan Li3Huahua Jian4Lu Fan5Rui Zhang6Xiang Xiao7Delong Meng8Xueduan Liu9Jianjun Wang10Huaqun Yin11Key Laboratory of Biometallurgy of Ministry of Education, School of Minerals Processing and Bioengineering, Central South UniversityEnvironmental Microbiomics Research Center, School of Environmental Science and Engineering, Sun Yat-sen UniversityState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of SciencesCollege of Agronomy, Hunan Agricultural UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityDepartment of Ocean Science and Engineering, Southern University of Science and TechnologyState Key Laboratory of Marine Environmental Science, The Institute of Marine Microbes and Ecospheres, Xiamen UniversityState Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityKey Laboratory of Biometallurgy of Ministry of Education, School of Minerals Processing and Bioengineering, Central South UniversityKey Laboratory of Biometallurgy of Ministry of Education, School of Minerals Processing and Bioengineering, Central South UniversityState Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and Limnology, Chinese Academy of SciencesKey Laboratory of Biometallurgy of Ministry of Education, School of Minerals Processing and Bioengineering, Central South UniversityAbstract Background Prokaryote-virus interactions play key roles in driving biogeochemical cycles. However, little is known about the drivers shaping their interaction network structures, especially from the host features. Here, we compiled 7656 species-level genomes in 39 prokaryotic phyla across environments globally and explored how their interaction specialization is constrained by host life history traits, such as growth rate. Results We first reported that host growth rate indicated by the reverse of minimal doubling time was negatively related to interaction specialization for host in host-provirus network across various ecosystems and taxonomy groups. Such a negative linear growth rate-specialization relationship (GrSR) was dependent on host optimal growth temperature (OGT), and stronger toward the two gradient ends of OGT. For instance, prokaryotic species with an OGT ≥ 40 °C showed a stronger GrSR (Pearson’s r = −0.525, P < 0.001). Significant GrSRs were observed with the presences of host genes in promoting the infection cycle at stages of adsorption, establishment, and viral release, but nonsignificant with the presence of immune systems, such as restriction-modification systems and CRISPR-Cas systems. Moreover, GrSR strength was increased with the presence of temperature-dependent lytic switches, which was also confirmed by mathematical modeling. Conclusions Together, our results advance our understanding of the interactions between prokaryotes and proviruses and highlight the importance of host growth rate in interaction specialization during lysogenization. Video Abstracthttps://doi.org/10.1186/s40168-022-01288-xHost-virus interactionGrowth rateSpecializationTemperatureInfection cycleGenetic traits |
| spellingShingle | Zhenghua Liu Qingyun Yan Chengying Jiang Juan Li Huahua Jian Lu Fan Rui Zhang Xiang Xiao Delong Meng Xueduan Liu Jianjun Wang Huaqun Yin Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits Microbiome Host-virus interaction Growth rate Specialization Temperature Infection cycle Genetic traits |
| title | Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits |
| title_full | Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits |
| title_fullStr | Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits |
| title_full_unstemmed | Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits |
| title_short | Growth rate determines prokaryote-provirus network modulated by temperature and host genetic traits |
| title_sort | growth rate determines prokaryote provirus network modulated by temperature and host genetic traits |
| topic | Host-virus interaction Growth rate Specialization Temperature Infection cycle Genetic traits |
| url | https://doi.org/10.1186/s40168-022-01288-x |
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