Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications
Abstract Background Candidate Phyla Radiation (CPR) represents a unique superphylum characterized by ultra-small cell size and symbiotic lifestyle. Although CPR bacteria have been identified in varied environments, their broader distribution, associations with hosts, and ecological roles remain larg...
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2025-04-01
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| Online Access: | https://doi.org/10.1186/s40168-025-02077-y |
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| author | Yu He Shiyan Zhuo Meng Li Jie Pan Yongguang Jiang Yidan Hu Robert A. Sanford Qin Lin Weimin Sun Na Wei Shuming Peng Zhou Jiang Shuyi Li Yongzhe Li Yiran Dong Liang Shi |
| author_facet | Yu He Shiyan Zhuo Meng Li Jie Pan Yongguang Jiang Yidan Hu Robert A. Sanford Qin Lin Weimin Sun Na Wei Shuming Peng Zhou Jiang Shuyi Li Yongzhe Li Yiran Dong Liang Shi |
| author_sort | Yu He |
| collection | DOAJ |
| description | Abstract Background Candidate Phyla Radiation (CPR) represents a unique superphylum characterized by ultra-small cell size and symbiotic lifestyle. Although CPR bacteria have been identified in varied environments, their broader distribution, associations with hosts, and ecological roles remain largely unexplored. To address these knowledge gaps, a serpentinite-like environment was selected as a simplified model system to investigate the CPR communities in hyperalkaline environments and their association with hosts in extreme conditions. Additionally, the enzymatic activity, global distribution, and evolution of the CPR-derived genes encoding essential metabolites (e.g., folate or vitamin B9) were analyzed and assessed. Results In the highly alkaline serpentinite-like ecosystem (pH = 10.9–12.4), metagenomic analyses of the water and sediment samples revealed that CPR bacteria constituted 1.93–34.8% of the microbial communities. Metabolic reconstruction of 12 high-quality CPR metagenome-assembled genomes (MAGs) affiliated to the novel taxa from orders UBA6257, UBA9973, and Paceibacterales suggests that these bacteria lack the complete biosynthetic pathways for amino acids, lipids, and nucleotides. Notably, the CPR bacteria commonly harbored the genes associated with essential folate cofactor biosynthesis and metabolism, including dihydrofolate reductase (folA), serine hydroxymethyltransferase (glyA), and methylenetetrahydrofolate reductase (folD). Additionally, two presumed auxotrophic hosts, incapable of forming tetrahydrofolate (THF) due to the absence of folA, were identified as potential hosts for some CPR bacteria harboring folA genes. The functionality of these CPR-derived folA genes was experimentally verified by heterologous expression in the folA-deletion mutant Escherichia coli MG1655 ΔfolA. Further assessment of the available CPR genomes (n = 4,581) revealed that the genes encoding the proteins for the synthesis of bioactive folate derivatives (e.g., folA, glyA, and/or folD genes) were present in 90.8% of the genomes examined. It suggests potential widespread metabolic complementarity in folate biosynthesis between CPR and their hosts. Conclusions This finding deepens our understanding of the mechanisms of CPR-host symbiosis, providing novel insight into essential cofactor-dependent mutualistic CPR-host interactions. Our observations suggest that CPR bacteria may contribute to auxotrophic organisms and indirectly influence biogeochemical processes. Video Abstract |
| format | Article |
| id | doaj-art-89f086188e36447fa0a92e7b92e6209e |
| institution | OA Journals |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | BMC |
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| spelling | doaj-art-89f086188e36447fa0a92e7b92e6209e2025-08-20T02:11:42ZengBMCMicrobiome2049-26182025-04-0113111510.1186/s40168-025-02077-yCandidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implicationsYu He0Shiyan Zhuo1Meng Li2Jie Pan3Yongguang Jiang4Yidan Hu5Robert A. Sanford6Qin Lin7Weimin Sun8Na Wei9Shuming Peng10Zhou Jiang11Shuyi Li12Yongzhe Li13Yiran Dong14Liang Shi15School of Environmental Studies, China University of Geosciences (Wuhan)School of Environmental Studies, China University of Geosciences (Wuhan)Archaeal Biology Centre, Synthetic Biology Research Center, Shenzhen Key Laboratory of Marine Microbiome Engineering, Key Laboratory of Marine Microbiome Engineering of Guangdong Higher Education Institutes, Institute for Advanced Study, Shenzhen UniversityArchaeal Biology Centre, Synthetic Biology Research Center, Shenzhen Key Laboratory of Marine Microbiome Engineering, Key Laboratory of Marine Microbiome Engineering of Guangdong Higher Education Institutes, Institute for Advanced Study, Shenzhen UniversitySchool of Environmental Studies, China University of Geosciences (Wuhan)School of Environmental Studies, China University of Geosciences (Wuhan)Department of Earth Science & Environmental Change, University of Illinois Urbana-ChampaignShanghai Biozeron Biological Technology Co. Ltd.Guangdong Institute of Eco-Environmental and Soil ScienceDepartment of Civil and Environmental Engineering, University of Illinois Urbana-ChampaignInstitute of Ecological Environment, Chengdu University of TechnologySchool of Environmental Studies, China University of Geosciences (Wuhan)School of Environmental Studies, China University of Geosciences (Wuhan)School of Environmental Studies, China University of Geosciences (Wuhan)School of Environmental Studies, China University of Geosciences (Wuhan)School of Environmental Studies, China University of Geosciences (Wuhan)Abstract Background Candidate Phyla Radiation (CPR) represents a unique superphylum characterized by ultra-small cell size and symbiotic lifestyle. Although CPR bacteria have been identified in varied environments, their broader distribution, associations with hosts, and ecological roles remain largely unexplored. To address these knowledge gaps, a serpentinite-like environment was selected as a simplified model system to investigate the CPR communities in hyperalkaline environments and their association with hosts in extreme conditions. Additionally, the enzymatic activity, global distribution, and evolution of the CPR-derived genes encoding essential metabolites (e.g., folate or vitamin B9) were analyzed and assessed. Results In the highly alkaline serpentinite-like ecosystem (pH = 10.9–12.4), metagenomic analyses of the water and sediment samples revealed that CPR bacteria constituted 1.93–34.8% of the microbial communities. Metabolic reconstruction of 12 high-quality CPR metagenome-assembled genomes (MAGs) affiliated to the novel taxa from orders UBA6257, UBA9973, and Paceibacterales suggests that these bacteria lack the complete biosynthetic pathways for amino acids, lipids, and nucleotides. Notably, the CPR bacteria commonly harbored the genes associated with essential folate cofactor biosynthesis and metabolism, including dihydrofolate reductase (folA), serine hydroxymethyltransferase (glyA), and methylenetetrahydrofolate reductase (folD). Additionally, two presumed auxotrophic hosts, incapable of forming tetrahydrofolate (THF) due to the absence of folA, were identified as potential hosts for some CPR bacteria harboring folA genes. The functionality of these CPR-derived folA genes was experimentally verified by heterologous expression in the folA-deletion mutant Escherichia coli MG1655 ΔfolA. Further assessment of the available CPR genomes (n = 4,581) revealed that the genes encoding the proteins for the synthesis of bioactive folate derivatives (e.g., folA, glyA, and/or folD genes) were present in 90.8% of the genomes examined. It suggests potential widespread metabolic complementarity in folate biosynthesis between CPR and their hosts. Conclusions This finding deepens our understanding of the mechanisms of CPR-host symbiosis, providing novel insight into essential cofactor-dependent mutualistic CPR-host interactions. Our observations suggest that CPR bacteria may contribute to auxotrophic organisms and indirectly influence biogeochemical processes. Video Abstracthttps://doi.org/10.1186/s40168-025-02077-yCandidate phylum radiation (CPR)FolateEssential cofactorsMutualismDihydrofolate reductase |
| spellingShingle | Yu He Shiyan Zhuo Meng Li Jie Pan Yongguang Jiang Yidan Hu Robert A. Sanford Qin Lin Weimin Sun Na Wei Shuming Peng Zhou Jiang Shuyi Li Yongzhe Li Yiran Dong Liang Shi Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications Microbiome Candidate phylum radiation (CPR) Folate Essential cofactors Mutualism Dihydrofolate reductase |
| title | Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications |
| title_full | Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications |
| title_fullStr | Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications |
| title_full_unstemmed | Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications |
| title_short | Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications |
| title_sort | candidate phyla radiation cpr bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications |
| topic | Candidate phylum radiation (CPR) Folate Essential cofactors Mutualism Dihydrofolate reductase |
| url | https://doi.org/10.1186/s40168-025-02077-y |
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