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

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 and Jin-tian Li ()
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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

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-47214-7

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