Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages
Abstract Phosphorus (P) limitation of ecosystem processes is widespread in terrestrial habitats. While a few auxiliary metabolic genes (AMGs) in bacteriophages from aquatic habitats are reported to have the potential to enhance P-acquisition ability of their hosts, little is known about the diversit...
| Main Authors: | , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-04-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-47214-7 |
| _version_ | 1797219678578278400 |
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| author | Jie-Liang Liang Shi-wei Feng Jing-li Lu Xiao-nan Wang Feng-lin Li Yu-qian Guo Shen-yan Liu Yuan-yue Zhuang Sheng-ji Zhong Jin Zheng Ping Wen Xinzhu Yi Pu Jia Bin Liao Wen-sheng Shu Jin-tian Li |
| author_facet | Jie-Liang Liang Shi-wei Feng Jing-li Lu Xiao-nan Wang Feng-lin Li Yu-qian Guo Shen-yan Liu Yuan-yue Zhuang Sheng-ji Zhong Jin Zheng Ping Wen Xinzhu Yi Pu Jia Bin Liao Wen-sheng Shu Jin-tian Li |
| author_sort | Jie-Liang Liang |
| collection | DOAJ |
| description | Abstract Phosphorus (P) limitation of ecosystem processes is widespread in terrestrial habitats. While a few auxiliary metabolic genes (AMGs) in bacteriophages from aquatic habitats are reported to have the potential to enhance P-acquisition ability of their hosts, little is known about the diversity and potential ecological function of P-acquisition genes encoded by terrestrial bacteriophages. Here, we analyze 333 soil metagenomes from five terrestrial habitat types across China and identify 75 viral operational taxonomic units (vOTUs) that encode 105 P-acquisition AMGs. These AMGs span 17 distinct functional genes involved in four primary processes of microbial P-acquisition. Among them, over 60% (11/17) have not been reported previously. We experimentally verify in-vitro enzymatic activities of two pyrophosphatases and one alkaline phosphatase encoded by P-acquisition vOTUs. Thirty-six percent of the 75 P-acquisition vOTUs are detectable in a published global topsoil metagenome dataset. Further analyses reveal that, under certain circumstances, the identified P-acquisition AMGs have a greater influence on soil P availability and are more dominant in soil metatranscriptomes than their corresponding bacterial genes. Overall, our results reinforce the necessity of incorporating viral contributions into biogeochemical P cycling. |
| first_indexed | 2024-04-24T12:37:28Z |
| format | Article |
| id | doaj.art-941829322dbe4c85b055edbed0cd4823 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-04-24T12:37:28Z |
| publishDate | 2024-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-941829322dbe4c85b055edbed0cd48232024-04-07T11:24:33ZengNature PortfolioNature Communications2041-17232024-04-0115111510.1038/s41467-024-47214-7Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophagesJie-Liang Liang0Shi-wei Feng1Jing-li Lu2Xiao-nan Wang3Feng-lin Li4Yu-qian Guo5Shen-yan Liu6Yuan-yue Zhuang7Sheng-ji Zhong8Jin Zheng9Ping Wen10Xinzhu Yi11Pu Jia12Bin Liao13Wen-sheng Shu14Jin-tian Li15Institute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversitySchool of Life Sciences, Sun Yat-sen UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityInstitute of Ecological Science, Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal UniversityAbstract Phosphorus (P) limitation of ecosystem processes is widespread in terrestrial habitats. While a few auxiliary metabolic genes (AMGs) in bacteriophages from aquatic habitats are reported to have the potential to enhance P-acquisition ability of their hosts, little is known about the diversity and potential ecological function of P-acquisition genes encoded by terrestrial bacteriophages. Here, we analyze 333 soil metagenomes from five terrestrial habitat types across China and identify 75 viral operational taxonomic units (vOTUs) that encode 105 P-acquisition AMGs. These AMGs span 17 distinct functional genes involved in four primary processes of microbial P-acquisition. Among them, over 60% (11/17) have not been reported previously. We experimentally verify in-vitro enzymatic activities of two pyrophosphatases and one alkaline phosphatase encoded by P-acquisition vOTUs. Thirty-six percent of the 75 P-acquisition vOTUs are detectable in a published global topsoil metagenome dataset. Further analyses reveal that, under certain circumstances, the identified P-acquisition AMGs have a greater influence on soil P availability and are more dominant in soil metatranscriptomes than their corresponding bacterial genes. Overall, our results reinforce the necessity of incorporating viral contributions into biogeochemical P cycling.https://doi.org/10.1038/s41467-024-47214-7 |
| spellingShingle | Jie-Liang Liang Shi-wei Feng Jing-li Lu Xiao-nan Wang Feng-lin Li Yu-qian Guo Shen-yan Liu Yuan-yue Zhuang Sheng-ji Zhong Jin Zheng Ping Wen Xinzhu Yi Pu Jia Bin Liao Wen-sheng Shu Jin-tian Li Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages Nature Communications |
| title | Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages |
| title_full | Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages |
| title_fullStr | Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages |
| title_full_unstemmed | Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages |
| title_short | Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages |
| title_sort | hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages |
| url | https://doi.org/10.1038/s41467-024-47214-7 |
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