Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter
Candidatus Accumulibacter, a prominent polyphosphate-accumulating organism (PAO) in wastewater treatment, plays a crucial role in enhanced biological phosphorus removal (EBPR). The genetic underpinnings of its polyphosphate accumulation capabilities, however, remain largely unknown. Here, we conduct...
| Main Authors: | , , , , , , , , |
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| Format: | Journal Article |
| Language: | English |
| Published: |
2024
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| Online Access: | https://hdl.handle.net/10356/175746 |
| _version_ | 1811687067413905408 |
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| author | Xie, Xiaojing Deng, Xuhan. Chen, Liping Yuan, Jing Chen, Hang Wei, Chaohai Liu, Xianghui Wuertz, Stefan Qiu, Guanglei |
| author2 | School of Civil and Environmental Engineering |
| author_facet | School of Civil and Environmental Engineering Xie, Xiaojing Deng, Xuhan. Chen, Liping Yuan, Jing Chen, Hang Wei, Chaohai Liu, Xianghui Wuertz, Stefan Qiu, Guanglei |
| author_sort | Xie, Xiaojing |
| collection | NTU |
| description | Candidatus Accumulibacter, a prominent polyphosphate-accumulating organism (PAO) in wastewater treatment, plays a crucial role in enhanced biological phosphorus removal (EBPR). The genetic underpinnings of its polyphosphate accumulation capabilities, however, remain largely unknown. Here, we conducted a comprehensive genomic analysis of Ca. Accumulibacter-PAOs and their relatives within the Rhodocyclaceae family, identifying 124 core genes acquired via horizontal gene transfer (HGT) at its least common ancestor. Metatranscriptomic analysis of an enrichment culture of Ca. Accumulibacter revealed active transcription of 44 of these genes during an EBPR cycle, notably including the polyphosphate kinase 2 (PPK2) gene instead of the commonly recognized polyphosphate kinase 1 (PPK1) gene. Intriguingly, the phosphate regulon (Pho) genes showed minimal transcriptions, pointing to a distinctive fact of Pho dysregulation, where PhoU, the phosphate signaling complex protein, was not regulating the high-affinity phosphate transport (Pst) system, resulting in continuous phosphate uptake. To prevent phosphate toxicity, Ca. Accumulibacter utilized the laterally acquired PPK2 to condense phosphate into polyphosphate, resulting in the polyphosphate-accumulating feature. This study provides novel insights into the evolutionary emergence of the polyphosphate-accumulating trait in Ca. Accumulibacter, offering potential advancements in understanding the PAO phenotype in the EBPR process. |
| first_indexed | 2024-10-01T05:10:25Z |
| format | Journal Article |
| id | ntu-10356/175746 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T05:10:25Z |
| publishDate | 2024 |
| record_format | dspace |
| spelling | ntu-10356/1757462024-05-10T15:35:04Z Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter Xie, Xiaojing Deng, Xuhan. Chen, Liping Yuan, Jing Chen, Hang Wei, Chaohai Liu, Xianghui Wuertz, Stefan Qiu, Guanglei School of Civil and Environmental Engineering Singapore Centre for Environmental Life Sciences and Engineering (SCELSE) Earth and Environmental Sciences Candidatus Accumulibacter Comparative genomics Candidatus Accumulibacter, a prominent polyphosphate-accumulating organism (PAO) in wastewater treatment, plays a crucial role in enhanced biological phosphorus removal (EBPR). The genetic underpinnings of its polyphosphate accumulation capabilities, however, remain largely unknown. Here, we conducted a comprehensive genomic analysis of Ca. Accumulibacter-PAOs and their relatives within the Rhodocyclaceae family, identifying 124 core genes acquired via horizontal gene transfer (HGT) at its least common ancestor. Metatranscriptomic analysis of an enrichment culture of Ca. Accumulibacter revealed active transcription of 44 of these genes during an EBPR cycle, notably including the polyphosphate kinase 2 (PPK2) gene instead of the commonly recognized polyphosphate kinase 1 (PPK1) gene. Intriguingly, the phosphate regulon (Pho) genes showed minimal transcriptions, pointing to a distinctive fact of Pho dysregulation, where PhoU, the phosphate signaling complex protein, was not regulating the high-affinity phosphate transport (Pst) system, resulting in continuous phosphate uptake. To prevent phosphate toxicity, Ca. Accumulibacter utilized the laterally acquired PPK2 to condense phosphate into polyphosphate, resulting in the polyphosphate-accumulating feature. This study provides novel insights into the evolutionary emergence of the polyphosphate-accumulating trait in Ca. Accumulibacter, offering potential advancements in understanding the PAO phenotype in the EBPR process. Published version This research was supported by the National Natural Science Foundation of China (52270035 and 51808297), the Natural Science Foundation of Guangdong Province (2021A1515010494), the Guangzhou Key Research and Development Program (2023B03J1334), and the Pearl River Talent Recruitment Program (2019QN01L125). 2024-05-06T01:36:27Z 2024-05-06T01:36:27Z 2024 Journal Article Xie, X., Deng, X., Chen, L., Yuan, J., Chen, H., Wei, C., Liu, X., Wuertz, S. & Qiu, G. (2024). Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter. Environmental Science and Ecotechnology, 20, 100353-. https://dx.doi.org/10.1016/j.ese.2023.100353 2666-4984 https://hdl.handle.net/10356/175746 10.1016/j.ese.2023.100353 2-s2.0-85181038663 20 100353 en Environmental Science and Ecotechnology © 2023 The Authors. Published by Elsevier B.V. on behalf of Chinese Society for Environmental Sciences, Harbin Institute of Technology, Chinese Research Academy of Environmental Sciences. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). application/pdf |
| spellingShingle | Earth and Environmental Sciences Candidatus Accumulibacter Comparative genomics Xie, Xiaojing Deng, Xuhan. Chen, Liping Yuan, Jing Chen, Hang Wei, Chaohai Liu, Xianghui Wuertz, Stefan Qiu, Guanglei Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter |
| title | Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter |
| title_full | Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter |
| title_fullStr | Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter |
| title_full_unstemmed | Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter |
| title_short | Integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of Ca. Accumulibacter |
| title_sort | integrated genomics provides insights into the evolution of the polyphosphate accumulation trait of ca accumulibacter |
| topic | Earth and Environmental Sciences Candidatus Accumulibacter Comparative genomics |
| url | https://hdl.handle.net/10356/175746 |
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