Register      Login
Soil Research Soil Research Society
Soil, land care and environmental research
RESEARCH ARTICLE

Alpine meadow degradation decreases soil P availability by altering phoD-harbouring bacterial diversity

Yanuo Zou A B , Xiangtao Wang C , Jie Wang D , Lu Zhang A B , Lirong Liao A B , Guobin Liu A B , Zilin Song E and Chao Zhang https://orcid.org/0000-0003-2647-2922 A B *
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Shaanxi, 712100, P. R. China.

B Institute of Soil and Water Conservation, Chinese Academy of Science, Shaanxi, 712100, P. R. China.

C College of Animal Science, Tibet Agriculture and Animal Husbandry University, Nyingchi, 860000, P. R. China.

D College of Forestry, Guizhou University, Guiyang, 550025, P. R. China.

E College of Natural Resources and Environment, Northwest A&F University, Shaanxi, 712100, P. R. China.

* Correspondence to: zhangchao1985@nwafu.edu.cn

Handling Editor: Sander Bruun

Soil Research 62, SR23133 https://doi.org/10.1071/SR23133
Submitted: 12 July 2023  Accepted: 18 April 2024  Published: 21 May 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Soil degradation is usually accompanied by significant changes in phosphorus (P) availability, which complicates soil management. However, the effect of ecosystem degradation on soil P availability remains poorly understood, especially in the alpine ecosystem, which is one of the most understudied and vulnerable terrestrial habitats of the planet.

Aims

Assess the effect of meadow degradation on soil P availability in the alpine ecosystem.

Methods

Changes in soil P-related properties, phoD-harbouring bacterial communities, and alkaline phosphatase levels were investigated in four alpine meadows along a degradation gradient (non-degraded, lightly degraded, moderately degraded, and severely degraded) on the Tibetan Plateau.

Key results

We found meadow degradation reduced alkaline phosphatase activity by 6.3–11.22% and soil P availability by 27.1–42.4% compared to the respective values in the non-degraded meadows, but this negative impact was only observed in moderately and severely degraded meadows. Meadow degradation caused a P limitation on the phoD-harbouring community and a decline in the abundance of phoD genes and diversity of phoD-harbouring bacterial communities, with an increase in oligotrophic groups (e.g. Actinobacteria) and a reduction in copiotrophic groups (e.g. Proteobacteria). The degradation-induced reduction in soil C supply and plant biomass decreased soil P availability by lowering the activity of alkaline phosphatases, which are closely associated with phoD-harbouring bacterial structure and diversity. Alloactinosynnema and Actinomadura were identified as the key taxa contributing to alkaline phosphatases activity.

Conclusions

Alpine meadow degradation decreases soil P availability by altering phoD-harbouring bacterial diversity.

Implications

Our results revealed the mechanisms of decreased P availability during alpine meadow degradation, which can guide the restoration of degraded meadow ecosystems.

Keywords: alkaline phosphatase, amplicon sequencing, grassland ecosystem, land degradation, phoD genes, phosphate-solubilizing bacteria, phosphorus availability, soil nutrients.

References

Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant, Cell & Environment 24(12), 1337-1344.
| Crossref | Google Scholar |

Alori ET, Glick BR, Babalola OO (2017) Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Frontiers in Microbiology 8, 971.
| Crossref | Google Scholar | PubMed |

Bergkemper F, Schöler A, Engel M, Lang F, Krüger J, Schloter M, Schulz S (2016) Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems. Environmental Microbiology 18(6), 1988-2000.
| Crossref | Google Scholar | PubMed |

Brady N, Weil R (2008) ‘Soil water: characteristics and behavior.’ pp. 177–217. (Prentice Hall)

Chen CR, Condron LM, Davis MR, Sherlock RR (2002) Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biology and Biochemistry 34(4), 487-499.
| Crossref | Google Scholar |

Chen H, Ju P, Zhu Q, Xu X, Wu N, Gao Y, Feng X, Tian J, Niu S, Zhang Y, Peng C, Wang Y (2022) Carbon and nitrogen cycling on the Qinghai–Tibetan Plateau. Nature Reviews Earth & Environment 3(10), 701-716.
| Crossref | Google Scholar |

Colvan S, Syers J, O’Donnell A (2001) Effect of long-term fertiliser use on acid and alkaline phosphomonoesterase and phosphodiesterase activities in managed grassland. Biology and Fertility of Soils 34(4), 258-263.
| Crossref | Google Scholar |

Dai Z, Liu G, Chen H, Chen C, Wang J, Ai S, Wei D, Li D, Ma B, Tang C, Brookes PC, Xu J (2020) Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. The ISME Journal 14(3), 757-770.
| Crossref | Google Scholar | PubMed |

Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6), 1354-1364.
| Crossref | Google Scholar | PubMed |

Fishwe RF, Binkley D (Eds) (2012) Forest biogeochemistry. In ‘Ecology and management of forest soils’. pp. 99–137. (John Wiley & Sons, Ltd)

Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology 60, 579-598.
| Crossref | Google Scholar |

Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biology and Biochemistry 85, 119-129.
| Crossref | Google Scholar |

Hu Y, Xia Y, Sun Q, Liu K, Chen X, Ge T, Zhu B, Zhu Z, Zhang Z, Su Y (2018) Effects of long-term fertilization on phoD-harboring bacterial community in Karst soils. Science of The Total Environment 628, 53-63.
| Crossref | Google Scholar | PubMed |

Huang L-M, Jia X-X, Zhang G-L, Shao M-A (2017) Soil organic phosphorus transformation during ecosystem development: a review. Plant and Soil 417(1–2), 17-42.
| Crossref | Google Scholar |

Kageyama H, Tripathi K, Rai AK, Cha-Um S, Waditee-Sirisattha R, Takabe T (2011) An alkaline phosphatase/phosphodiesterase, PhoD, induced by salt stress and secreted out of the cells of Aphanothece halophytica, a Halotolerant Cyanobacterium. Applied Environmental Microbiology 77(15), 5178-5183.
| Crossref | Google Scholar | PubMed |

Lai C, Li C, Peng F, Xue X, You Q, Zhang W, Ma S (2021) Plant community change mediated heterotrophic respiration increase explains soil organic carbon loss before moderate degradation of alpine meadow. Land Degradation & Development 32(18), 5322-5333.
| Crossref | Google Scholar |

Li J, Xie T, Zhu H, Zhou J, Li C, Xiong W, Xu L, Wu Y, He Z, Li X (2021a) Alkaline phosphatase activity mediates soil organic phosphorus mineralization in a subalpine forest ecosystem. Geoderma 404, 115376.
| Crossref | Google Scholar |

Li H, Qiu Y, Yao T, Han D, Gao Y, Zhang J, Ma Y, Zhang H, Yang X (2021b) Nutrients available in the soil regulate the changes of soil microbial community alongside degradation of alpine meadows in the northeast of the Qinghai-Tibet Plateau. Science of The Total Environment 792, 148363.
| Crossref | Google Scholar |

Li W, Wang J, Jiang L, Lv G, Hu D, Wu D, Yang X (2023) Rhizosphere effect and water constraint jointly determined the roles of microorganism in soil phosphorus cycling in arid desert regions. Catena 222, 106809.
| Crossref | Google Scholar |

Liang JL, Liu J, Jia P, Yang TT, Zeng QW, Zhang SC, Liao B, Shu WS, Li JT (2020) Novel phosphate-solubilizing bacteria enhance soil phosphorus cycling following ecological restoration of land degraded by mining. The ISME Journal 14(6), 1600-1613.
| Crossref | Google Scholar | PubMed |

Lin XA, Hc A, Cl B, Cw C, Nh D, Sh E, My A, Cw F, Jw G, Sz A (2021) The importance of rare versus abundant phoD-harboring subcommunities in driving soil alkaline phosphatase activity and available P content in Chinese steppe ecosystems. Soil Biology and Biochemistry 164, 108491.
| Crossref | Google Scholar |

Luo G, Ling N, Nannipieri P, Chen H, Raza W, Wang M, Guo S, Shen Q (2017) Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biology Fertility of Soils 53, 375-388.
| Crossref | Google Scholar |

Luo G, Sun B, Li L, Li M, Liu M, Zhu Y, Guo S, Ling N, Shen Q (2019a) Understanding how long-term organic amendments increase soil phosphatase activities: Insight into phoD- and phoC-harboring functional microbial populations. Soil Biology and Biochemistry 139, 107632.
| Crossref | Google Scholar |

Luo R, Fan J, Wang W, Luo J, Kuzyakov Y, He JS, Chu H, Ding W (2019b) Nitrogen and phosphorus enrichment accelerates soil organic carbon loss in alpine grassland on the Qinghai-Tibetan Plateau. Science of The Total Environment 650(Pt 1), 303-312.
| Crossref | Google Scholar | PubMed |

MacDougall AS, McCann KS, Gellner G, Turkington RJN (2013) Diversity loss with persistent human disturbance increases vulnerability to ecosystem collapse. Nature 494(7435), 86-89.
| Crossref | Google Scholar | PubMed |

McLaren TI, Smernik RJ, McLaughlin MJ, McBeath TM, Kirby JK, Simpson RJ, Guppy CN, Doolette AL, Richardson AE (2015) Complex forms of soil organic phosphorus–a major component of soil phosphorus. Environmental Science & Technology 49(22), 13238-13245.
| Crossref | Google Scholar | PubMed |

Niu K, He J-S, Lechowicz MJ (2016) Foliar phosphorus content predicts species relative abundance in P-limited Tibetan alpine meadows. Perspectives in Plant Ecology, Evolution and Systematics 22, 47-54.
| Crossref | Google Scholar |

Peng X, Wang W (2016) Stoichiometry of soil extracellular enzyme activity along a climatic transect in temperate grasslands of northern China. Soil Biology and Biochemistry 98, 74-84.
| Crossref | Google Scholar |

Peng Y, Duan Y, Huo W, Xu M, Yang X, Wang X, Wang B, Blackwell MSA, Feng G (2021) Soil microbial biomass phosphorus can serve as an index to reflect soil phosphorus fertility. Biology and Fertility of Soils 57(5), 657-669.
| Crossref | Google Scholar |

Peng Y, Duan Y, Huo W, Zhang Z, Huang D, Xu M, Wang X, Yang X, Wang B, Kuzyakov Y, Feng G (2022) C:P stoichiometric imbalance between soil and microorganisms drives microbial phosphorus turnover in the rhizosphere. Biology and Fertility of Soils 58(4), 421-433.
| Crossref | Google Scholar |

Preece C, Farré-Armengol G, Penuelas J (2020) Drought is a stronger driver of soil respiration and microbial communities than nitrogen or phosphorus addition in two Mediterranean tree species. Science of The Total Environment 735, 139554.
| Crossref | Google Scholar | PubMed |

Ragot SA, Kertesz MA, Bunemann EK (2015) phoD Alkaline Phosphatase Gene Diversity in Soil. Appl Environ Microbiol 81(20), 7281-7289.
| Crossref | Google Scholar | PubMed |

Richardson AE, Simpson R (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant physiology 156(3), 989-996.
| Crossref | Google Scholar |

Saha S, Prakash V, Kundu S, Kumar N, Mina BL (2008) Soil enzymatic activity as affected by long term application of farm yard manure and mineral fertilizer under a rainfed soybean–wheat system in N-W Himalaya. European Journal of Soil Biology 44(3), 309-315.
| Crossref | Google Scholar |

Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462, 795-798.
| Crossref | Google Scholar |

Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biology Biochemistry 61, 69-75.
| Crossref | Google Scholar |

Turner BL, Blackwell MSA (2013) Isolating the influence of pH on the amounts and forms of soil organic phosphorus. European Journal of Soil Science 64(2), 249-259.
| Crossref | Google Scholar |

Turner BL, McKelvie ID, Haygarth PM (2002) Characterisation of water-extractable soil organic phosphorus by phosphatase hydrolysis. Soil Biology and Biochemistry 34(1), 27-35.
| Crossref | Google Scholar |

Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry 19(6), 703-707.
| Crossref | Google Scholar |

Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications 20(1), 5-15.
| Crossref | Google Scholar | PubMed |

Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15(1), 1-19.
| Crossref | Google Scholar |

Wan W, He D, Li X, Xing Y, Liu S, Ye L, Njoroge DM, Yang Y (2021a) Adaptation of phoD-harboring bacteria to broader environmental gradients at high elevations than at low elevations in the Shennongjia primeval forest. Geoderma 401, 115210.
| Crossref | Google Scholar |

Wan W, He D, Li X, Xing Y, Liu S, Ye L, Yang Y (2021b) Linking rare and abundant phoD-harboring bacteria with ecosystem multifunctionality in subtropical forests: From community diversity to environmental adaptation. Science of The Total Environment 796, 148943.
| Crossref | Google Scholar | PubMed |

Wang W, Wang Q, Wang H (2006) The effect of land management on plant community composition, species diversity, and productivity of alpine Kobersia steppe meadow. Ecological Research 21, 181-187.
| Crossref | Google Scholar |

Wang M, Zhang C, Chen S, Zhang Y, Li Y, Xin X, Wang X, Yan R (2022) Effects of grazing intensity on the carbon, nitrogen and phosphorus content, stoichiometry and storage of plant functional groups in a meadow steppe. Agronomy 12(12), 3057.
| Crossref | Google Scholar |

Wang L, Zhang H, Xu C, Yuan J, Xu XJ, Wang JD, Zhang YC (2023) Long-term nitrogen fertilization and sweetpotato cultivation in the wheat-sweetpotato rotation system decrease alkaline phosphomonoesterase activity by regulating soil phoD-harboring bacteria communities. Science of The Total Environment 900, 165916.
| Crossref | Google Scholar |

Wei X, Hu Y, Razavi BS, Zhou J, Shen J, Nannipieri P, Wu J, Ge T (2019) Rare taxa of alkaline phosphomonoesterase-harboring microorganisms mediate soil phosphorus mineralization. Soil Biology and Biochemistry 131, 62-70.
| Crossref | Google Scholar |

Wiegand S, Jogler M, Jogler C (2018) On the maverick Planctomycetes. FEMS Microbiology Reviews 42(6), 739-760.
| Crossref | Google Scholar | PubMed |

Xu YD, Dong SK, Shen H, Xiao JN, Li S, Gao XX, Wu SN (2021) Degradation significantly decreased the ecosystem multifunctionality of three alpine grasslands: evidences from a large-scale survey on the Qinghai-Tibetan Plateau. Journal of Mountain Science 18(2), 357-366.
| Crossref | Google Scholar |

Yan N, Marschner P, Cao W, Zuo C, Qin W (2015) Influence of salinity and water content on soil microorganisms. International Soil and Water Conservation Research 3(4), 316-323.
| Crossref | Google Scholar |

Yan T, Lü X-T, Zhu J-J, Yang K, Yu L-Z, Gao T (2018) Changes in nitrogen and phosphorus cycling suggest a transition to phosphorus limitation with the stand development of larch plantations. Plant and Soil 422(1–2), 385-396.
| Crossref | Google Scholar |

Yang H, Gou X, Xue B, Ma W, Kuang W, Tu Z, Gao L, Yin D, Zhang J (2023) Research on the change of alpine ecosystem service value and its sustainable development path. Ecological Indicators 146, 109893.
| Crossref | Google Scholar |

Zaidi A, Khan M, Ahemad M, Oves M (2009) Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiologica et Immunologica Hungarica 56(3), 263-284.
| Crossref | Google Scholar | PubMed |

Zhang C, Liu G, Xue S, Wang G (2016) Soil bacterial community dynamics reflect changes in plant community and soil properties during the secondary succession of abandoned farmland in the Loess Plateau. Soil Biology and Biochemistry 97, 40-49.
| Crossref | Google Scholar |

Zhou H, Zhou L, Zhao X, Liu W, Li Y, Gu S, Zhou X (2006) Stability of alpine meadow ecosystem on the Qinghai-Tibetan Plateau. Chinese Science Bulletin 51(3), 320-327.
| Crossref | Google Scholar |

Zhou H, Zhang D, Jiang Z, Sun P, Xiao H, Yuxin W, Chen J (2018) Changes in the soil microbial communities of alpine steppe at Qinghai-Tibetan Plateau under different degradation levels. Science of The Total Environment 651(Pt 2), 2281-2291.
| Crossref | Google Scholar | PubMed |

Zhu X, Zhao X, Lin Q, Li G (2021) Distribution characteristics of phoD-harbouring bacterial community structure and its roles in phosphorus transformation in steppe soils in Northern China. Journal of Soil Science and Plant Nutrition 21(2), 1531-1541.
| Crossref | Google Scholar |