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Rare microbial taxa rather than phoD gene abundance determine hotspots of alkaline phosphomonoesterase activity in the karst rhizosphere soil

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Abstract

The spatial distribution of alkaline phosphomonoesterase (ALP) activity in the rhizosphere and bulk soil of three plants (Zea mays, Medicago sativa, and Cyperus rotundus) grown in a karst soil (pH 8.27) was visualized using in situ soil zymography. According to the zymogram images, we identified and precisely collected soil samples from hotspots and non-hotspots of ALP activity, and then analyzed the phoD genes that encoded alkaline phosphomonoesterase and assessed the microbial community. The results showed that (1) the phoD abundance in the plant types varied and was highest in the alfalfa and lowest in the maize; (2) Proteobacteria dominated the phoD-harboring microbes in the rhizosphere and Actinobacteria dominated the phoD-harboring microbes in the bulk soil, and (3) the ALP activity was positively correlated with the relative abundance of the diazotrophic Azotobacter, but negatively correlated with the phoD gene abundance, microbial community richness, and diversity. By coupling zymography and microbial molecular approaches, we identified hotspots of enzymatic and microbial activity in rhizosphere soil and evaluated the relative contributions from potential active microorganisms. We found that the function of specific phoD-harboring microorganisms in these hotspots differed depending on the plant in the soil, which had implications for phosphorus (P) management in P-limited karst soils. The results also suggested that free-living N2-fixing bacteria (Azotobacter) might promote ALP activity, thereby emphasizing vital linkages between, and coupling of, the soil nutrient cycles.

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Funding

This study was supported by the Science Centre project of National Natural Science Foundation of China (Grant Nos. 31988102), and state key and the general programs of the National Natural Science Foundation of China (Grant Nos. 41830860, 41877091, 41571130043), and the National Environmental Research Council of the UK (Grant No. NE/N007603/1).

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Authors and Affiliations

  1. Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100101, China

    Shuang Liu & Xinyu Zhang

  2. College of Resources and Environment, University of Chinese Academy of Sciences, Beijing, 100190, China

    Shuang Liu & Xinyu Zhang

  3. Geography, College of Life and Environmental Sciences, University of Exeter, Rennes Drive, Exeter, EX4 4RJ, UK

    Jennifer A. J. Dungait & Timothy A. Quine

  4. Department of Soil and Plant Microbiome, Institute of Phytopathology, University of Kiel, Kiel, Germany

    Bahar S. Razavi

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  1. Shuang Liu
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Table S1

The primers used for qPCR and corresponding amplification cycling conditions (DOCX 15 kb)

Fig. S1

Sampling diagram with maize as an example (a) zymogram image showing differences in enzyme activity around the roots. (b) precise sampling hotspots and non-hotspots soils in rhizoboxes. The yellow ellipse represents the bulk soil and the red ellipse represents the rhizosphere (DOCX 2276 kb)

Fig. S2

Distributions of phosphomonoesterase activities in maize, alfalfa, and sedge roots from (a) the root tip upward and (b) the root center outward (DOCX 164 kb)

Fig. S3

DNA concentration (ng g dry soil−1) in the rhizosphere and bulk soils of maize, alfalfa, and sedge rhizoboxes. Upper case letters indicate significant differences (p < 0.05) between different plant species in their rhizosphere and bulk soils, respectively. Lower letters indicate the significant differences (p < 0.05) between soils of the same plant species (DOCX 42 kb)

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Liu, S., Zhang, X., Dungait, J.A.J. et al. Rare microbial taxa rather than phoD gene abundance determine hotspots of alkaline phosphomonoesterase activity in the karst rhizosphere soil. Biol Fertil Soils 57, 257–268 (2021). https://doi.org/10.1007/s00374-020-01522-4

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