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Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages

Author

Listed:
  • Jie-Liang Liang

    (South China Normal University)

  • Shi-wei Feng

    (South China Normal University)

  • Jing-li Lu

    (South China Normal University)

  • Xiao-nan Wang

    (South China Normal University)

  • Feng-lin Li

    (South China Normal University)

  • Yu-qian Guo

    (South China Normal University)

  • Shen-yan Liu

    (South China Normal University)

  • Yuan-yue Zhuang

    (South China Normal University)

  • Sheng-ji Zhong

    (South China Normal University)

  • Jin Zheng

    (South China Normal University)

  • Ping Wen

    (South China Normal University)

  • Xinzhu Yi

    (South China Normal University)

  • Pu Jia

    (South China Normal University)

  • Bin Liao

    (Sun Yat-sen University)

  • Wen-sheng Shu

    (South China Normal University)

  • Jin-tian Li

    (South China Normal University)

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.

Suggested Citation

  • 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-s, 2024. "Hidden diversity and potential ecological function of phosphorus acquisition genes in widespread terrestrial bacteriophages," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47214-7
    DOI: 10.1038/s41467-024-47214-7
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    References listed on IDEAS

    as
    1. Enqing Hou & Yiqi Luo & Yuanwen Kuang & Chengrong Chen & Xiankai Lu & Lifen Jiang & Xianzhen Luo & Dazhi Wen, 2020. "Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    2. Mohammad Bahram & Falk Hildebrand & Sofia K. Forslund & Jennifer L. Anderson & Nadejda A. Soudzilovskaia & Peter M. Bodegom & Johan Bengtsson-Palme & Sten Anslan & Luis Pedro Coelho & Helery Harend & , 2018. "Structure and function of the global topsoil microbiome," Nature, Nature, vol. 560(7717), pages 233-237, August.
    3. Shaoming Gao & David Paez-Espino & Jintian Li & Hongxia Ai & Jieliang Liang & Zhenhao Luo & Jin Zheng & Hao Chen & Wensheng Shu & Linan Huang, 2022. "Patterns and ecological drivers of viral communities in acid mine drainage sediments across Southern China," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Kristopher Kieft & Zhichao Zhou & Rika E. Anderson & Alison Buchan & Barbara J. Campbell & Steven J. Hallam & Matthias Hess & Matthew B. Sullivan & David A. Walsh & Simon Roux & Karthik Anantharaman, 2021. "Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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    Cited by:

    1. Zongzhi Wu & Tang Liu & Qian Chen & Tianyi Chen & Jinyun Hu & Liyu Sun & Bingxue Wang & Wenpeng Li & Jinren Ni, 2024. "Unveiling the unknown viral world in groundwater," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

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