Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study
ABSTRACT The dynamics of the structure of polyhydroxyalkanoate-producing mixed microbial cultures (PHA-MMCs) during enrichment and maintenance is an unsolved problem. The effect of phages has been proposed as a cause of dynamic changes in community structure, but evidence is lacking. To address this...
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American Society for Microbiology
2025-04-01
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| Series: | mSystems |
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| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00200-25 |
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| author | Jian Yao Yan Zeng Xia Hong Meng Wang Quan Zhang Yating Chen Min Gou Zi-Yuan Xia Yue-Qin Tang |
| author_facet | Jian Yao Yan Zeng Xia Hong Meng Wang Quan Zhang Yating Chen Min Gou Zi-Yuan Xia Yue-Qin Tang |
| author_sort | Jian Yao |
| collection | DOAJ |
| description | ABSTRACT The dynamics of the structure of polyhydroxyalkanoate-producing mixed microbial cultures (PHA-MMCs) during enrichment and maintenance is an unsolved problem. The effect of phages has been proposed as a cause of dynamic changes in community structure, but evidence is lacking. To address this question, five PHA-MMCs were enriched, and biological samples were sampled temporally to study the interactions between phage and bacterial members by combining metagenomics and metatranscriptomics. A total of 963 metagenome-assembled genomes (MAGs) and 4,294 phage operational taxonomic units (pOTUs) were assembled from bulk metagenomic data. The dynamic changes in the structure of phage and bacterial communities were remarkably consistent. Structural equation modeling analysis showed that phages could infect and lyse dominant species to vacate ecological niches for other species, resulting in a community succession state in which dominant species alternated. Seven key auxiliary metabolic genes (AMGs), phaC, fadJ, acs, ackA, phbB, acdAB, and fadD, potentially contributing to PHA synthesis were identified from phage sequences. Importantly, these AMGs were transcribed, indicating that they were in an active expression state. The meta-analysis provides the first catalog of phages in PHA-MMCs and the AMGs they carry, as well as how they affect the dynamic changes in bacterial communities. This study provides a reference for subsequent studies on understanding and regulating the microbial community structure of open microbial systems.IMPORTANCEThe synthesis of biodegradable plastic PHA from organic waste through mixed microbial cultures (PHA-MMCs), at extremely low cost, has the potential for expanded production. However, the dynamics of dominant species in PHA-MMCs are poorly understood. Our results demonstrate for the first time the impact of phages on the structure of bacterial communities in the PHA-MMCs. There are complex interactions between the PHA producers (e.g., Azomonas, Paracoccus, and Thauera) and phages (e.g., Casadabanvirus and unclassified Hendrixvirinae). Phage communities can regulate the activity and structure of bacterial communities. In addition, the AMGs related to PHA synthesis may hitchhike during phage-host infection cycles, enabling their dissemination across bacterial communities, and phages may act as a critical genetic reservoir for bacterial members, facilitating access to PHA synthesis-related functional traits. This study highlights the impact of phages on bacterial community structure, suggesting that phages have the potential to be used as a tool for better controlling the microbial community structure of PHA-MMCs. |
| format | Article |
| id | doaj-art-d4e709584e6b4c99a74c9340908aadbf |
| institution | OA Journals |
| issn | 2379-5077 |
| language | English |
| publishDate | 2025-04-01 |
| publisher | American Society for Microbiology |
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| series | mSystems |
| spelling | doaj-art-d4e709584e6b4c99a74c9340908aadbf2025-08-20T02:12:20ZengAmerican Society for MicrobiologymSystems2379-50772025-04-0110410.1128/msystems.00200-25Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics studyJian Yao0Yan Zeng1Xia Hong2Meng Wang3Quan Zhang4Yating Chen5Min Gou6Zi-Yuan Xia7Yue-Qin Tang8College of Architecture and Environment, Sichuan University, , Chengdu, Sichuan, ChinaCollege of Architecture and Environment, Sichuan University, , Chengdu, Sichuan, ChinaSinopec Shanghai Engineering Co. Ltd., Shanghai, ChinaSinopec (Dalian) Research Institute of Petroleum and Petrochemicals Co. Ltd., Dalian, Liaoning, ChinaSinopec (Dalian) Research Institute of Petroleum and Petrochemicals Co. Ltd., Dalian, Liaoning, ChinaSichuan Environmental Protection Key Laboratory of Organic Wastes Valorization, Chengdu, Sichuan, ChinaCollege of Architecture and Environment, Sichuan University, , Chengdu, Sichuan, ChinaCollege of Architecture and Environment, Sichuan University, , Chengdu, Sichuan, ChinaCollege of Architecture and Environment, Sichuan University, , Chengdu, Sichuan, ChinaABSTRACT The dynamics of the structure of polyhydroxyalkanoate-producing mixed microbial cultures (PHA-MMCs) during enrichment and maintenance is an unsolved problem. The effect of phages has been proposed as a cause of dynamic changes in community structure, but evidence is lacking. To address this question, five PHA-MMCs were enriched, and biological samples were sampled temporally to study the interactions between phage and bacterial members by combining metagenomics and metatranscriptomics. A total of 963 metagenome-assembled genomes (MAGs) and 4,294 phage operational taxonomic units (pOTUs) were assembled from bulk metagenomic data. The dynamic changes in the structure of phage and bacterial communities were remarkably consistent. Structural equation modeling analysis showed that phages could infect and lyse dominant species to vacate ecological niches for other species, resulting in a community succession state in which dominant species alternated. Seven key auxiliary metabolic genes (AMGs), phaC, fadJ, acs, ackA, phbB, acdAB, and fadD, potentially contributing to PHA synthesis were identified from phage sequences. Importantly, these AMGs were transcribed, indicating that they were in an active expression state. The meta-analysis provides the first catalog of phages in PHA-MMCs and the AMGs they carry, as well as how they affect the dynamic changes in bacterial communities. This study provides a reference for subsequent studies on understanding and regulating the microbial community structure of open microbial systems.IMPORTANCEThe synthesis of biodegradable plastic PHA from organic waste through mixed microbial cultures (PHA-MMCs), at extremely low cost, has the potential for expanded production. However, the dynamics of dominant species in PHA-MMCs are poorly understood. Our results demonstrate for the first time the impact of phages on the structure of bacterial communities in the PHA-MMCs. There are complex interactions between the PHA producers (e.g., Azomonas, Paracoccus, and Thauera) and phages (e.g., Casadabanvirus and unclassified Hendrixvirinae). Phage communities can regulate the activity and structure of bacterial communities. In addition, the AMGs related to PHA synthesis may hitchhike during phage-host infection cycles, enabling their dissemination across bacterial communities, and phages may act as a critical genetic reservoir for bacterial members, facilitating access to PHA synthesis-related functional traits. This study highlights the impact of phages on bacterial community structure, suggesting that phages have the potential to be used as a tool for better controlling the microbial community structure of PHA-MMCs.https://journals.asm.org/doi/10.1128/msystems.00200-25polyhydroxyalkanoates (PHAs)mixed microbial cultures (MMCs)community assemblymicrobial community structure dynamicsphages-bacteria interactionsphages-host dynamics |
| spellingShingle | Jian Yao Yan Zeng Xia Hong Meng Wang Quan Zhang Yating Chen Min Gou Zi-Yuan Xia Yue-Qin Tang Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study mSystems polyhydroxyalkanoates (PHAs) mixed microbial cultures (MMCs) community assembly microbial community structure dynamics phages-bacteria interactions phages-host dynamics |
| title | Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study |
| title_full | Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study |
| title_fullStr | Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study |
| title_full_unstemmed | Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study |
| title_short | Phages-bacteria interactions underlying the dynamics of polyhydroxyalkanoate-producing mixed microbial cultures via meta-omics study |
| title_sort | phages bacteria interactions underlying the dynamics of polyhydroxyalkanoate producing mixed microbial cultures via meta omics study |
| topic | polyhydroxyalkanoates (PHAs) mixed microbial cultures (MMCs) community assembly microbial community structure dynamics phages-bacteria interactions phages-host dynamics |
| url | https://journals.asm.org/doi/10.1128/msystems.00200-25 |
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