Abstract
[Aims] The goal was to evaluate the effect of phosphorus mining on the endophytic bacterial community of surrounding crops and vegetables and screen beneficial bacteria. [Methods] 16S rRNA sequencing was used to assess endophytic bacterial diversity, community, and metabolic function variations in surrounding plants, including Glycine max, Triticum aestivum, and Lactuca sativa. [Results] The results showed that phosphorus mining caused a decline in the endophytic bacterial diversity of plants, including the Shannon and Simpson indices (P < 0.05). Rhizobium was significantly enriched in lettuce, soybean, and wheat roots in the phosphate mining area compared with corresponding samples from a nonphosphate mining area (P < 0.05). The metabolic function prediction based on Phylogenetic Investigation of Communities by Reconstruction of Unobserved States showed that endophytic bacteria in lettuce, soybean, and wheat roots developed various strategies to cope with phosphorus mining stress. We further isolated 11 endophytic bacteria from the three plant types, of which Enterobacter sp. P35, Pseudomonas aeruginosa P33, and Rhizobium pusense P25 showed strong resistance to multiple heavy metals. Several endophytic bacteria, including Pseudomonas aeruginosa P33, Sphingomonas panni P15, and Bacillus cereus P3, showed multiple growth-promoting properties for plants. [Conclusions] To our knowledge, this is the first study to examine the effects of phosphate mining on endophytic bacteria in human food sources (vegetables and crops), providing a comprehensive understanding of the ecological effects of phosphate mining. The results also highlight the need to pay attention to the easily neglected effect of phosphorus mining on the microecology and provide a basis for screening bacteria for remediation.
This is a preview of subscription content, access via your institution.








Data Availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Afzal I, Shinwari ZK, Sikandar S, Shahzad S (2019) Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiol Res 221:36–49
Almeida A, Loy A, Hofmann H (2018) ggplot2 Compatible Quantile-Quantile Plots in R. R J 10:248–261
Alvarez A, Catalano SA, Amoroso MJ (2013) Heavy metal resistant strains are widespread along Streptomyces phylogeny. Mol Phylogenet Evol 66:1083–1088
Arshad M, Naqvi N, Gul I, Yaqoob K, Bilal M, Kallerhoff J (2020) Lead phytoextraction by Pelargonium hortorum: Comparative assessment of EDTA and DIPA for Pb mobility and toxicity. Sci Total Environ 748:141496
Asaf S, Numan M, Khan AL, Al-Harrasi A (2020) Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol 40:138–152
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium, Nat Genet 25:25–29
Bao Z, Feng H, Tu W, Li L, Li Q (2022) Method and mechanism of chromium removal from soil: a systematic review. Environ Sci Pollut Res Int 29:35501–35517
Bao Z, Wang X, Wang Q, Zou L, Peng L, Li L, Tu W, Li Q (2023) A novel method of domestication combined with ARTP to improve the reduction ability of Bacillus velezensis to Cr(VI). J Environ Chem Eng 11:109091
Bothe H, Slomka A (2017) Divergent biology of facultative heavy metal plants. J Plant Physiol 219:45–61
Caicedo-Montoya C, Gomez-Roman MP, Vazquez-Hernandez M, Mora-Rincon RA, Rodriguez-Luna SD, Rodriguez-Sanoja R, Sanchez S (2021) Evolutionary genomics and biosynthetic potential of novel environmental Actinobacteria. Appl Microbiol Biotechnol 105:8805–8822
Canedo-Arguelles M, Brucet S, Carrasco S, Flor-Arnau N, Ordeix M, Ponsa S, Coring E (2017) Effects of potash mining on river ecosystems: An experimental study. Environ Pollut 224:759–770
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Chen C, Lei W, Lu M, Zhang J, Zhang Z, Luo C, Chen Y, Hong Q, Shen Z (2016) Characterization of Cu(II) and Cd(II) resistance mechanisms in Sphingobium sp. PHE-SPH and Ochrobactrum sp. PHE-OCH and Their Potential Application in the Bioremediation of Heavy Metal-Phenanthrene Co-Contaminated Sites, Environ Sci Pollut Res Int 23:6861–6872
Chen J, Zhang J, Qu M, Yang L, Zhao Y, Huang B (2021) Pollution characteristics and risk assessment of soil heavy metals in the areas affected by the mining of metal-bearing minerals in Southwest China. Bull Environ Contam Toxicol 107:1070–1079
de Araujo SN, Ramos SJ, Martins GC, Teixeira RA, de Souza ES, Sahoo PK, Fernandes AR, Gastauer M, Caldeira CF, Souza-Filho PWM, Dall’Agnol R (2022) Copper mining in the eastern Amazon: an environmental perspective on potentially toxic elements. Environ Geochem Health 44:1767–1781
deMelo Pereira GV, Magalhaes KT, Lorenzetii ER, Souza TP, Schwan RF (2012) A multiphasic approach for the identification of endophytic bacterial in strawberry fruit and their potential for plant growth promotion. Microb Ecol 63:405–417
Douglas GM, Beiko RG, Langille MGI (1849) Predicting the Functional Potential of the Microbiome from Marker Genes Using PICRUSt. Methods Mol Biol 2018:169–177
Dubey A, Malla MA, Kumar A, Dayanandan S, Khan ML (2020) Plants endophytes: unveiling hidden agenda for bioprospecting toward sustainable agriculture. Crit Rev Biotechnol 40:1210–1231
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998
El Zrelli R, Rabaoui L, Daghbouj N, Abda H, Castet S, Josse C, van Beek P, Souhaut M, Michel S, Bejaoui N, Courjault-Rade P (2018) Characterization of phosphate rock and phosphogypsum from Gabes phosphate fertilizer factories (SE Tunisia): high mining potential and implications for environmental protection. Environ Sci Pollut Res Int 25:14690–14702
Espiritu EQ, Claveria RJR, Bernadas PJC (2022) Assessment of surface water quality and mercury levels from Artisanal and small-scale gold mining (ASGM) along Acupan River, Benguet, Philippines. Environ Geochem Health 44:3655–3676
Fan M, Liu Z, Nan L, Wang E, Chen W, Lin Y, Wei G (2018) Isolation, characterization, and selection of heavy metal-resistant and plant growth-promoting endophytic bacteria from root nodules of Robinia pseudoacacia in a Pb/Zn mining area. Microbiol Res 217:51–59
Filippelli GM (2011) Phosphate rock formation and marine phosphorus geochemistry: the deep time perspective. Chemosphere 84:759–766
Gabay T, Rotem G, Gillor O, Ziv Y (2022) Understanding changes in biocrust communities following phosphate mining in the Negev Desert. Environ Res 207:112200
Gong D, Ye F, Pang C, Lu Z, Shang C (2020) Isolation and Characterization of Pseudomonas sp. Cr13 and Its Application in Removal of Heavy Metal Chromium. Curr Microbiol 77:3661–3670
Hao H, Ge D, Wen Y, Lv Y, Chen W (2022) Probabilistic health risk assessment of inorganic arsenic and some heavy metals in rice produced from a typical multi-mining county, China. Environ Sci Pollut Res Int 29:11510–11523
Heusinkveld D, Ramirez-Andreotta MD, Rodriguez-Chavez T, Saez AE, Betterton E, Rine K (2021) Assessing Children’s Lead Exposure in an Active Mining Community Using the Integrated Exposure Uptake Biokinetic Model. Exposure and Health 13:517–533
Huang G, Gao R, You J, Zhu J, Fu Q, Hu H (2019) Oxalic acid activated phosphate rock and bone meal to immobilize Cu and Pb in mine soils. Ecotoxicol Environ Saf 174:401–407
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30
Karmakar R, Bindiya S, Hariprasad P (2019) Convergent evolution in bacteria from multiple origins under antibiotic and heavy metal stress, and endophytic conditions of host plant. Sci Total Environ 650:858–867
Khan S, Afzal M, Iqbal S, Khan QM (2013) Plant-bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332
Kiani T, Khan SA, Noureen N, Yasmin T, Zakria M, Ahmed H, Mehboob F, Farrakh S (2019) Isolation and characterization of culturable endophytic bacterial community of stripe rust-resistant and stripe rust-susceptible Pakistani wheat cultivars. Int Microbiol 22:191–201
Lata R, Chowdhury S, Gond SK, White JF Jr (2018) Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol 66:268–276
Li Q, Luo Y, Sha A, Xiao W, Xiong Z, Chen X, He J, Peng L, Zou L (2023) Analysis of synonymous codon usage patterns in mitochondrial genomes of nine Amanita species. Front Microbiol 14Z:1134228
Li Q, Xiang P, Zhang T, Wu Q, Bao Z, Tu W, Li L, Zhao C (2022a) The effect of phosphate mining activities on rhizosphere bacterial communities of surrounding vegetables and crops. Sci Total Environ 821:153479
Li Q, Wu Q, Zhang T, Xiang P, Bao Z, Tu W, Li L, Wang Q (2022b) Phosphate mining activities affect crop rhizosphere fungal communities. Sci Total Environ 838:156196
Li X, Yang Q, Wang L, Song C, Chen L, Zhang J, Liang Y (2022c) Using Caenorhabditis elegans to assess the ecological health risks of heavy metals in soil and sediments around Dabaoshan Mine, China. Environ Sci Pollut Res Int 29:16332–16345
Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner Plant Values: Diversity Colonization and Benefits from Endophytic Bacteria. Front Microbiol 8:2552
Liu DS, Wang CQ, Mei XD, Zhang C (2019a) An effective treatment method for phosphogypsum. Environ Sci Pollut Res Int 26:30533–30539
Liu LH, Yuan T, An QL, Yang MY, Mao XY, Mo CH, Tan ZY, Peng GX (2019b) Azotobacter bryophylli sp. nov., isolated from the succulent plant Bryophyllum pinnatum. Int J Syst Evol Micr 69:1986–1992
Liu Y, Wang P, Gojenko B, Yu J, Wei L, Luo D, Xiao T (2021a) A review of water pollution arising from agriculture and mining activities in Central Asia: Facts, causes and effects. Environ Pollut 291:118209
Liu B, He Z, Liu R, Montenegro AC, Ellis M, Li Q, Baligar VC (2021b) Comparative effectiveness of activated dolomite phosphate rock and biochar for immobilizing cadmium and lead in soils. Chemosphere 266:129202
Louw I (2020) Potential radiological impact of the phosphate industry in South Africa on the public and the environment (Paper 1). J Environ Radioact 217:106214
Magnan A, Duvat V (2015) Environment: phosphate mining risks atoll culture. Nature 522:156
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963
Martinez-Escobar DF, Mallela J (2019) Assessing the impacts of phosphate mining on coral reef communities and reef development. Sci Total Environ 692:1257–1266
Naamala J, Jaiswal SK, Dakora FD (2016) Antibiotics Resistance in Rhizobium: Type, Process, Mechanism and Benefit for Agriculture. Curr Microbiol 72:804–816
Natasha N, Shahid M, Bibi I, Iqbal J, Khalid S, Murtaza B, Bakhat HF, Farooq ABU, Amjad M, Hammad HM, Niazi NK, Arshad M (2022) Zinc in soil-plant-human system: A data-analysis review. Sci Total Environ 808:152024
Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14:1504
Othman I, Al-Masri MS (2007) Impact of phosphate industry on the environment: a case study. Appl Radiat Isot 65:131–141
Pinski A, Betekhtin A, Hupert-Kocurek K, Mur LAJ, Hasterok R (2019) Defining the genetic basis of plant(-)endophytic bacteria interactions. Int J Mol Sci 20:1947
Phieler R, Voit A, Kothe E (2014) Microbially supported phytoremediation of heavy metal contaminated soils: strategies and applications. Adv Biochem Eng Biotechnol 141:211–235
Photolo MM, Sitole L, Mavumengwana V, Tlou MG (2021) Genomic and physiological investigation of heavy metal resistance from plant endophytic methylobacterium radiotolerans MAMP 4754, isolated from combretum erythrophyllum. Int J Environ Res Public Health 18:997
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590-596
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181
Roman-Ponce B, Ramos-Garza J, Vasquez-Murrieta MS, Rivera-Orduna FN, Chen WF, Yan J, Estrada-de Los Santos P, Wang ET (2016) Cultivable endophytic bacteria from heavy metal(loid)-tolerant plants. Arch Microbiol 198:941–956
Ruthrof KX, Steel E, Misra S, McComb J, O’Hara G, Hardy G, Howieson J (2018) Transitioning from phosphate mining to agriculture: Responses to urea and slow release fertilizers for Sorghum bicolor. Sci Total Environ 625:1–7
Salmi A, Boulila F (2021) Heavy metals multi-tolerant Bradyrhizobium isolated from mercury mining region in Algeria. J Environ Manage 289:112547
Santoyo G, Moreno-Hagelsieb G, Orozco-MosquedaMdel C, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99
Sharma P, Kumar S (2021) Bioremediation of heavy metals from industrial effluents by endophytes and their metabolic activity: Recent advances. Bioresour Technol 339:125589
Sharma RK, Barot K, Archana G (2020) Root colonization by heavy metal resistant Enterobacter and its influence on metal induced oxidative stress on Cajanus cajan. J Sci Food Agric 100:1532–1540
Taule C, Vaz-Jauri P, Battistoni F (2021) Insights into the early stages of plant-endophytic bacteria interaction. World J Microbiol Biotechnol 37:13
Tayibi H, Choura M, Lopez FA, Alguacil FJ, Lopez-Delgado A (2009) Environmental impact and management of phosphogypsum. J Environ Manage 90:2377–2386
Tiwari S, Sarangi BK, Thul ST (2016) Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J Environ Manage 180:359–365
Tu W, Cao X, Cheng J, Li L, Zhang T, Wu Q, Xiang P, Shen C, Li Q (2022) Chinese Baijiu: the perfect works of microorganisms. Front Microbiol 13:919044
van Rhijn P, Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59:124–142
Vogel C, Hoffmann MC, Taube MC, Kruger O, Baran R, Adam C (2020) Uranium and thorium species in phosphate rock and sewage sludge ash based phosphorus fertilizers. J Hazard Mater 382:121100
Wang K, Lin Z, Zhang R (2016) Impact of phosphate mining and separation of mined materials on the hydrology and water environment of the Huangbai River basin, China. Sci Total Environ 543:347–356
Wang J, Liu J, Ling W, Huang Q, Gao Y (2017) Composite of PAH-degrading endophytic bacteria reduces contamination and health risks caused by PAHs in vegetables. Sci Total Environ 598:471–478
Wang S, Ji B, Su X, Li H, Dong C, Chen S, Zhu Y, Feng W (2020a) Isolation of endophytic bacteria from Rehmannia glutinosa Libosch and their potential to promote plant growth. J Gen Appl Microbiol 66:279–288
Wang Q, Li Q, Lin Y, Hou Y, Deng Z, Liu W, Wang H, Xia Z (2020b) Biochemical and genetic basis of cadmium biosorption by Enterobacter ludwigii LY6, isolated from industrial contaminated soil. Environ Pollut 264:114637
White JF, Kingsley KL, Zhang Q, Verma R, Obi N, Dvinskikh S, Elmore MT, Verma SK, Gond SK, Kowalski KP (2019) Review: Endophytic microbes and their potential applications in crop management. Pest Manag Sci 75:2558–2565
Wu J, Kamal N, Hao H, Qian C, Liu Z, Shao Y, Zhong X, Xu B (2019) Endophytic Bacillus megaterium BM18-2 mutated for cadmium accumulation and improving plant growth in Hybrid Pennisetum. Biotechnol Rep (Amst) 24:e00374
Wu Q, Li L, Xiang P, Zhang T, Peng L, Zou L, Li Q (2023) Phages in fermented foods: interactions and applications. Fermentation 9:201
Yang Y, Guo T, Jiao W (2018) Destruction processes of mining on water environment in the mining area combining isotopic and hydrochemical tracer. Environ Pollut 237:356–365
Yu Y, Xiong J, Liu R, He Z (2019) Release of Heavy Metals from Dolomite Phosphate Rock after Activation with Organic Agent. J Environ Qual 48:694–700
Yu Y, Li Z, Liu Y, Wang F, Liu Y, Zhao J, Li Y, Gao Y, Zhu N (2022) Roles of plant-associated microorganisms in regulating the fate of Hg in croplands: A perspective on potential pathways in maintaining sustainable agriculture. Sci Total Environ 834:155204
Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Biores Technol 98:2557–2561
Funding
This work was supported by the National Natural Science Foundation of China (grant no. 42107233), Sichuan Natural Science Foundation Project (2023NSFSC1229), the CAS Key Laboratory of Environmental and Applied Microbiology & Environmental Microbiology Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences (No. KLCAS-2021–3), and the Open Research Fund Program of the State Environmental Protection Key Laboratory of Food Chain Pollution Control (No. FC2021YB08).
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: Q.L., and C.Z. Analyzed the data: P.X., T.Z., Q.W., Z.B., L.L., and W.T. Wrote and reviewed the paper: Q.L., and P.X..
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflicts of interest.
Additional information
Responsible Editor: Stéphane Compant.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Fig. S1
Rarefaction curves of bacterial OTUs in different samples. Gma, endophytic bacteria associated with soybean roots from the nonphosphorus mining area; Lsa, endophytic bacteria associated with lettuce roots from the nonphosphorus mining area; Tae, endophytic bacteria associated with wheat roots from the nonphosphorus mining area; Gma.P, endophytic bacteria associated with soybean roots from the phosphorus mining area; Lsa.P, endophytic bacteria associated with lettuce roots from the phosphorus mining area; Tae.P, endophytic bacteria associated with wheat roots from the phosphorus mining area (DOC 525 KB)
Fig. S2
Unique and shared operational taxonomic units (OTUs) of different samples. Gma, endophytic bacteria associated with soybean roots from the nonphosphorus mining area; Lsa, endophytic bacteria associated with lettuce roots from the nonphosphorus mining area; Tae, endophytic bacteria associated with wheat roots from the nonphosphorus mining area; Gma.P, endophytic bacteria associated with soybean roots from the phosphorus mining area; Lsa.P, endophytic bacteria associated with lettuce roots from the phosphorus mining area; Tae.P, endophytic bacteria associated with wheat roots from the phosphorus mining area (DOC 1188 KB)
Fig. S3
Overall Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway annotation of endophytic bacteria from different samples (DOC 792 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, Q., Xiang, P., Li, L. et al. Phosphorus mining activities alter endophytic bacterial communities and metabolic functions of surrounding vegetables and crops. Plant Soil (2023). https://doi.org/10.1007/s11104-023-05961-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-023-05961-4