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Synergistic Impacts of Arsenic and Antimony Co-contamination on Diazotrophic Communities

  • Environmental Microbiology
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Abstract

Nitrogen (N) shortage poses a great challenge to the implementation of in situ bioremediation practices in mining-contaminated sites. Diazotrophs can fix atmospheric N2 into a bioavailable form to plants and microorganisms inhabiting adverse habitats. Increasing numbers of studies mainly focused on the diazotrophic communities in the agroecosystems, while those communities in mining areas are still not well understood. This study compared the variations of diazotrophic communities in composition and interactions in the mining areas with different extents of arsenic (As) and antimony (Sb) contamination. As and Sb co-contamination increased alpha diversities and the abundance of nifH encoding the dinitrogenase reductase, while inhibited the diazotrophic interactions and substantially changed the composition of communities. Based on the multiple lines of evidence (e.g., the enrichment analysis of diazotrophs, microbe-microbe network, and random forest regression), six diazotrophs (e.g., Sinorhizobium, Dechloromonas, Trichormus, Herbaspirillum, Desmonostoc, and Klebsiella) were identified as keystone taxa. Environment-microbe network and random forest prediction demonstrated that these keystone taxa were highly correlated with the As and Sb contamination fractions. All these results imply that the above-mentioned diazotrophs may be resistant to metal(loid)s.

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Data Availability

The datasets generated during the current study are available in the NCBI database under the project number PRJNA695517.

References

  1. Missimer TM, Teaf CM, Beeson WT, Maliva RG, Woolschlager J, Covert DJ (2018) Natural background and anthropogenic arsenic enrichment in Florida soils, surface water, and groundwater: a review with a discussion on public health risk. Int J Environ Res Public Health 15:2278. https://doi.org/10.3390/ijerph15102278

    Article  CAS  PubMed Central  Google Scholar 

  2. Hiller E, Lalinská B, Chovan M, Jurkovic L, Klimko T, Jankulár M, Hovorič R, Šottník P, Flakova R, Enišová Z, Ondrejková I (2012) Arsenic and antimony contamination of waters, stream sediments and soils in the vicinity of abandoned antimony mines in the Western Carpathians, Slovakia Editorial handling by. Appl Geochem 27:598–614. https://doi.org/10.1016/j.apgeochem.2011.12.005

    Article  CAS  Google Scholar 

  3. Wang J, Liu G, Wu H, Zhang T, Liu X, Li W (2018) Temporal-spatial variation and partitioning of dissolved and particulate heavy metal(loid)s in a river affected by mining activities in Southern China. Environ Sci Pollut Res Int 25:9828–9839. https://doi.org/10.1007/s11356-018-1322-x

    Article  CAS  PubMed  Google Scholar 

  4. Liu JL, Yao J, Wang F, Min N, Gu JH, Li ZF, Sunahara G, Duran R, Solevic-Knudsen T, Hudson-Edwards KA, Alakangas L (2019) Bacterial diversity in typical abandoned multi-contaminated nonferrous metal(loid) tailings during natural attenuation. Environ Pollut 247:98–107. https://doi.org/10.1016/j.envpol.2018.12.045

    Article  CAS  PubMed  Google Scholar 

  5. Fu Z, Wu F, Mo C, Deng Q, Meng W, Giesy JP (2016) Comparison of arsenic and antimony biogeochemical behavior in water, soil and tailings from Xikuangshan, China. Sci Total Environ 539:97–104. https://doi.org/10.1016/j.scitotenv.2015.08.146

    Article  CAS  PubMed  Google Scholar 

  6. Drahota P, Raus K, Rychlíková E, Rohovec J (2018) Bioaccessibility of As, Cu, Pb, and Zn in mine waste, urban soil, and road dust in the historical mining village of Kaňk, Czech Republic. Environ Geochem Health 40:1495–1512. https://doi.org/10.1007/s10653-017-9999-1

    Article  CAS  PubMed  Google Scholar 

  7. Sun X, Song B, Xu R, Zhang M, Gao P, Lin H, Sun W (2021) Root-associated (rhizosphere and endosphere) microbiomes of the Miscanthus sinensis and their response to the heavy metal contamination. J Environ Sci 104:387–398. https://doi.org/10.1016/j.jes.2020.12.019

    Article  CAS  Google Scholar 

  8. Xu R, Sun X, Häggblom MM, Dong Y, Zhang M, Yang Z, Xiao E, Xiao T, Gao P, Li B, Sun W (2021) Metabolic potentials of members of the class Acidobacteriia in metal-contaminated soils revealed by metagenomic analysis. Environ Microbiol. https://doi.org/10.1111/1462-2920.15612

    Article  PubMed  PubMed Central  Google Scholar 

  9. Sun W, Xiao E, Xiao T, Krumins V, Wang Q, Häggblom M, Dong Y, Tang S, Hu M, Li B, Xia B, Liu W (2017) Response of soil microbial communities to elevated antimony and arsenic contamination indicates the relationship between the innate microbiota and contaminant fractions. Environ Sci Technol 51:9165–9175. https://doi.org/10.1021/acs.est.7b00294

    Article  CAS  PubMed  Google Scholar 

  10. Lehr CR, Kashyap DR, McDermott TR (2007) New insights into microbial oxidation of antimony and arsenic. Appl Environ Microbiol 73:2386–2389. https://doi.org/10.1128/AEM.02789-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sundar S, Chakravarty J (2010) Antimony toxicity. Int J Environ Res Public Health 7:4267–4277. https://doi.org/10.3390/ijerph7124267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ojuederie OB, Babalola OO (2017) Microbial and plant-assisted bioremediation of heavy metal polluted environments: a review. Int J Environ Res Public Health 14. https://doi.org/10.3390/ijerph14121504

  13. Xiao E, Cui J, Sun W, Jiang S, Huang M, Kong D, Wu Q, Xiao T, Sun X, Ning Z (2021) Root microbiome assembly of As-hyperaccumulator Pteris vittata and its efficacy in arsenic requisition. Environ Microbiol 23:1959–1971. https://doi.org/10.1111/1462-2920.15299

    Article  CAS  PubMed  Google Scholar 

  14. Moynahan OS, Zabinski CA, Gannon JE (2002) Microbial community structure and carbon-utilization diversity in a mine tailings revegetation study. Restor Ecol 10:77–87. https://doi.org/10.1046/j.1526-100X.2002.10108.x

    Article  Google Scholar 

  15. Dobson A, Bradshaw A, Baker A (1997) Hopes for the future: restoration ecology and conservation biology. Science 277:515–522. https://doi.org/10.1126/science.277.5325.515

    Article  CAS  Google Scholar 

  16. Sun X, Kong T, Häggblom MM, Kolton M, Li F, Dong Y, Huang Y, Li B, Sun W (2020) Chemolithoautotropic diazotrophy dominates the nitrogen fixation process in mine tailings. Environ Sci Technol 54:6082–6093. https://doi.org/10.1021/acs.est.9b07835

    Article  CAS  PubMed  Google Scholar 

  17. Sun W, Sun X, Li B, Xu R, Young LY, Dong Y, Zhang M, Kong T, Xiao E, Wang Q (2020) Bacterial response to sharp geochemical gradients caused by acid mine drainage intrusion in a terrace: relevance of C, N, and S cycling and metal resistance. Environ Int 138:105601. https://doi.org/10.1016/j.envint.2020.105601

    Article  CAS  PubMed  Google Scholar 

  18. Titus JH, Bishop JG (2014) Propagule limitation and competition with nitrogen fixers limit conifer colonization during primary succession. J Veg Sci 25:990–1003. https://doi.org/10.1111/jvs.12155

    Article  Google Scholar 

  19. Wong M (2003) Ecological restoration of mine degraded soils, with emphasis on metal contaminated soils. Chemosphere 50:775–780. https://doi.org/10.1016/S0045-6535(02)00232-1

    Article  CAS  PubMed  Google Scholar 

  20. Huang L-N, Tang F-Z, Song Y-S, Wan C-Y, Wang S-L, Liu W, Shu W (2011) Biodiversity, abundance, and activity of nitrogen-fixing bacteria during primary succession on a copper mine tailings. FEMS Microbiol Ecol 78:439–450. https://doi.org/10.1111/j.1574-6941.2011.01178.x

    Article  CAS  PubMed  Google Scholar 

  21. Knelman J, Legg T, O’Neill S, Washenberger C, González A, Cleveland C, Nemergut D (2012) Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biol Biochem 46:172–180. https://doi.org/10.1016/j.soilbio.2011.12.001

    Article  CAS  Google Scholar 

  22. Li Y, Jia Z, Sun Q, Zhan J, Yang Y, Wang D (2016) Ecological restoration alters microbial communities in mine tailings profiles. Sci Rep 6:25193. https://doi.org/10.1038/srep25193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. McGrath S, Brookes PC, Giller K (1988) Effects of potentially toxic elements in soils derived from past applications of sewage sludge on nitrogen fixation by Trifolium Repens L. Soil Biol Biochem 20:415–424. https://doi.org/10.1016/0038-0717(88)90052-1

    Article  CAS  Google Scholar 

  24. Yadav OP, Shukla UC (1983) Effect of zinc on nodulation and nitrogen fixation in chickpea (Cicer arietinum L.). J Agric Sci 101:559–563. https://doi.org/10.1017/S0021859600038582

    Article  CAS  Google Scholar 

  25. Aziza K, Rais N, Elsass F, Duplay J, Fahli N, el ghachtouli N, (2017) Effects of long-term heavy metals contamination on soil microbial characteristics in calcareous agricultural lands (Saiss plain, North Morocco). J Mater Environ Sci 8:691–695

    Google Scholar 

  26. Pau R (1989) Nitrogenase without molybdenum. Trends Biochem Sci 14:183–186. https://doi.org/10.1016/0968-0004(89)90271-5

    Article  CAS  PubMed  Google Scholar 

  27. Angove H, Yoo S, Burgess B, Münck E (1997) Mössbauer and EPR evidence for an all-ferrous Fe4S4 cluster with S = 4 in the Fe protein of nitrogenase. J Am Chem Soc 119. https://doi.org/10.1021/ja9712837

  28. Chen LX, Li JT, Chen YT, Huang LN, Hua Z, Hu M, Shu W (2013) Shifts in microbial community composition and function in the acidification of a lead/zinc mine tailings. Environ Microbiol 15. https://doi.org/10.1111/1462-2920.12114

  29. Ledin M, Pedersen K (1996) The environmental impact of mine wastes—roles of microorganisms and their significance in treatment of mine wastes. Earth Sci Rev 41:67–108. https://doi.org/10.1016/0012-8252(96)00016-5

    Article  CAS  Google Scholar 

  30. Sun W, Xiao E, Häggblom M, Krumins V, Dong Y, Sun X, Li F, Wang Q, Li B, Yan B (2018) Bacterial survival strategies in an alkaline tailing site and the physiological mechanisms of dominant phylotypes as revealed by metagenomic analyses. Environ Sci Technol 52. https://doi.org/10.1021/acs.est.8b03853

  31. Zelaya-Molina LX, Hernández-Soto LM, Guerra-Camacho JE, Monterrubio-López R, Patiño-Siciliano A, Villa-Tanaca L, Hernández-Rodríguez C (2016) Ammonia-oligotrophic and diazotrophic heavy metal-resistant Serratia liquefaciens strains from pioneer plants and mine tailings. Microb Ecol 72:324–346. https://doi.org/10.1007/s00248-016-0771-3

    Article  CAS  PubMed  Google Scholar 

  32. Dyhrman S, Haley S (2011) Arsenate resistance in the unicellular marine diazotroph Crocosphaera watsonii. Front Microbiol 2:214. https://doi.org/10.3389/fmicb.2011.00214

    Article  PubMed  PubMed Central  Google Scholar 

  33. Pandey S, Rai R, Rai L (2011) Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteomics 75:921–937. https://doi.org/10.1016/j.jprot.2011.10.011

    Article  CAS  PubMed  Google Scholar 

  34. Glick B (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. https://doi.org/10.1016/j.biotechadv.2010.02.001

    Article  CAS  PubMed  Google Scholar 

  35. Chen W-M, Wu C-H, James E, Chang J-S (2008) Biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa pudica. J Hazard Mater 151:364–371. https://doi.org/10.1016/j.jhazmat.2007.05.082

    Article  CAS  PubMed  Google Scholar 

  36. Jiang C-y, Sheng X-F, Qian M, Wang Q-y (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164. https://doi.org/10.1016/j.chemosphere.2008.02.006

    Article  CAS  PubMed  Google Scholar 

  37. Nie L, Shah S, Rashid A, Burd G, Dixon DG, Glick B (2002) Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol Biochem 40:355–361. https://doi.org/10.1016/S0981-9428(02)01375-X

    Article  CAS  Google Scholar 

  38. Navarro-Noya YE, Hernández-Mendoza E, Morales-Jiménez J, Jan-Roblero J, Martínez-Romero E, Hernández-Rodríguez C (2012) Isolation and characterization of nitrogen fixing heterotrophic bacteria from the rhizosphere of pioneer plants growing on mine tailings. Appl Soil Ecol 62:52–60. https://doi.org/10.1016/j.apsoil.2012.07.011

  39. Andres J, Arsène-Ploetze F, Barbe V, Brochier-Armanet C, Cleiss-Arnold J, Coppée J-Y, Dillies M-A, Geist L, Joublin A, Koechler S, Lassalle F, Marchal M, Médigue C, Muller D, Nesme X, Plewniak F, Proux C, Ramírez-Bahena MH, Schenowitz C, Sismeiro O, Vallenet D, Santini JM, Bertin PN (2013) Life in an arsenic-containing gold mine: genome and physiology of the autotrophic arsenite-oxidizing bacterium Rhizobium sp. NT-26. Genome Biol Evol 5:934–953. https://doi.org/10.1093/gbe/evt061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hamamura N, Fukushima K, Itai T (2013) Identification of antimony- and arsenic-oxidizing bacteria associated with antimony mine tailing. Microbes Environ 28:257–263. https://doi.org/10.1264/jsme2.me12217

    Article  PubMed  PubMed Central  Google Scholar 

  41. Li W, Liu J, Hudson-Edwards KA (2020) Seasonal variations in arsenic mobility and bacterial diversity: the case study of Huangshui Creek, Shimen Realgar Mine, Hunan Province. China Sci Total Environ 749:142353. https://doi.org/10.1016/j.scitotenv.2020.142353

    Article  CAS  PubMed  Google Scholar 

  42. Li L, Tu H, Zhang S, Wu L, Wu M, Tang Y, Wu P (2019) Geochemical behaviors of antimony in mining-affected water environment (Southwest China). Environ Geochem Health 41:2397–2411. https://doi.org/10.1007/s10653-019-00285-8

    Article  CAS  PubMed  Google Scholar 

  43. Li L, Liu H, Li H (2018) Distribution and migration of antimony and other trace elements in a Karstic river system, Southwest China. Environ Sci Pollut Res Int 25:28061–28074. https://doi.org/10.1007/s11356-018-2837-x

    Article  CAS  PubMed  Google Scholar 

  44. Gao P, Song B, Xu R, Sun X, Lin H, Xu F, Li B, Sun W (2021) Structure and variation of root-associated bacterial communities of Cyperus rotundus L. in the contaminated soils around Pb/Zn mine sites. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-14595-x

    Article  Google Scholar 

  45. Wu F, Wang JT, Yang J, Li J (1987) Zheng YM (2016) Does arsenic play an important role in the soil microbial community around a typical arsenic mining area? Environmental pollution (Barking. Essex 213:949–956. https://doi.org/10.1016/j.envpol.2016.03.057

    Article  CAS  Google Scholar 

  46. She W, Jie Y, Xing H, Liu Y, Kang W, Wang D (2011) Heavy metal concentrations and bioaccumulations of ramie (Boehmeria nivea) growing on 3 mining areas in Shimen, Lengshuijiang and Liuyang of Hunan Provice. Acta Ecol Sin 874–881

  47. Wilson S, Lockwood P, Ashley P, Tighe M (2010) The chemistry and behaviour of antimony in the soil environment with comparisons to arsenic: a critical review. Environ Pollut 158:1169–1181. https://doi.org/10.1016/j.envpol.2009.10.045

    Article  CAS  PubMed  Google Scholar 

  48. Sun W, Xiao E, Kalin M, Krumins V, Dong Y, Zengping N, Liu T, Sun M, Zhao Y, Wu S, Mao J, Xiao T (2016) Remediation of antimony-rich mine waters: assessment of antimony removal and shifts in the microbial community of an onsite field-scale bioreactor. Environ Pollut 215:213–222. https://doi.org/10.1016/j.envpol.2016.05.008

    Article  CAS  PubMed  Google Scholar 

  49. Sun X, Kong T, Xu R, Li B, Sun W (2020) Comparative characterization of microbial communities that inhabit arsenic-rich and antimony-rich contaminated sites: responses to two different contamination conditions. Environ Pollut 260:114052. https://doi.org/10.1016/j.envpol.2020.114052

    Article  CAS  PubMed  Google Scholar 

  50. Yang Z, Hosokawa H, Kuroda M, Inoue D, Ike M (2020) Microbial antimonate reduction and removal potentials in river sediments. Chemosphere 266:129192. https://doi.org/10.1016/j.chemosphere.2020.129192

    Article  CAS  PubMed  Google Scholar 

  51. Xu R, Sun X, Han F, Li B, Xiao E, Xiao T, Yang Z, Sun W (2020) Impacts of antimony and arsenic co-contamination on the river sedimentary microbial community in an antimony-contaminated river. Sci Total Environ 713:136451. https://doi.org/10.1016/j.scitotenv.2019.136451

    Article  CAS  PubMed  Google Scholar 

  52. Fu Z, Wu F, Amarasiriwardena D, Mo C, Liu B, Zhu J, Deng Q, Liao H (2010) Antimony, arsenic and mercury in the aquatic environment and fish in a large antimony mining area in Hunan, China. Sci Total Environ 408:3403–3410. https://doi.org/10.1016/j.scitotenv.2010.04.031

    Article  CAS  PubMed  Google Scholar 

  53. Sun X, Li B, Han F, Xiao E, Xiao T, Sun W (2019) Impacts of arsenic and antimony co-contamination on sedimentary microbial communities in rivers with different pollution gradients. Microb Ecol 78:589–602

    Article  CAS  Google Scholar 

  54. Poly F, Monrozier LJ, Bally R (2001) Improvement in the RFLP procedure for studying the diversity of nifH genes in communities of nitrogen fixers in soil. Res Microbiol 152:95–103. https://doi.org/10.1016/S0923-2508(00)01172-4

    Article  CAS  PubMed  Google Scholar 

  55. Wang Q, Xie Z, Li F (2015) Using ensemble models to identify and apportion heavy metal pollution sources in agricultural soils on a local scale. Environ Pollut 206:227–235. https://doi.org/10.1016/j.envpol.2015.06.040

    Article  CAS  PubMed  Google Scholar 

  56. Csardi G, Nepusz T (2005) The igraph software package for complex network research. Inter J Complex Syst 1695, 1–9

  57. Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci 103:8577. https://doi.org/10.1073/pnas.0601602103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zhang J, Zhang N, Liu YX, Zhang X, Hu B, Qin Y, Xu H, Wang H, Guo X, Qian J, Wang W, Zhang P, Jin T, Chu C, Bai Y (2018) Root microbiota shift in rice correlates with resident time in the field and developmental stage. Sci China Life Sci 61:613–621. https://doi.org/10.1007/s11427-018-9284-4

    Article  PubMed  Google Scholar 

  59. Puri A, Padda KP, Chanway CP (2015) Can a diazotrophic endophyte originally isolated from lodgepole pine colonize an agricultural crop (corn) and promote its growth? Soil Biol Biochem 89:210–216. https://doi.org/10.1016/j.soilbio.2015.07.012

    Article  CAS  Google Scholar 

  60. Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource Annu Rev Environ Resour. Annual Reviews, Palo Alto, pp 97–125

  61. Ullah A, Mushtaq H, Ali H, Munis MF, Javed MT, Chaudhary HJ (2015) Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res Int 22:2505–2514. https://doi.org/10.1007/s11356-014-3699-5

    Article  CAS  PubMed  Google Scholar 

  62. Bormann B, Sidle RC (1990) Changes in productivity and distribution of nutrients in a chronosequence at Glacier Bay National Park, Alaska. J Ecol 561–578

  63. Matthews JA (1992) The ecology of recently-deglaciated terrain: a geoecological approach to glacier forelands. Cambridge University Press, Cambridge, UK

    Google Scholar 

  64. Walker LR, Del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, Cambridge

  65. Li B, Xu R, Sun X, Han F, Xiao E, Chen L, Qiu L, Sun W (2021) Microbiome–environment interactions in antimony-contaminated rice paddies and the correlation of core microbiome with arsenic and antimony contamination. Chemosphere 263:128227. https://doi.org/10.1016/j.chemosphere.2020.128227

    Article  CAS  PubMed  Google Scholar 

  66. Li Y, Wang M, Chen S (2021) Application of N2-fixing Paenibacillus triticisoli BJ-18 changes the compositions and functions of the bacterial, diazotrophic, and fungal microbiomes in the rhizosphere and root/shoot endosphere of wheat under field conditions. Biol Fertil Soils. https://doi.org/10.1007/s00374-020-01528-y

    Article  Google Scholar 

  67. Palumbo-Roe B, Wragg J, Cave M (2015) Linking selective chemical extraction of iron oxyhydroxides to arsenic bioaccessibility in soil. Environ Pollut 207:256–265. https://doi.org/10.1016/j.envpol.2015.09.026

    Article  CAS  PubMed  Google Scholar 

  68. Johnson D (2003) Chemical and microbiological characteristics of mineral spoils and drainage waters at abandoned coal and metal mines. Water Air Soil Pollut Focus 3:47–66. https://doi.org/10.1023/A:1022107520836

    Article  CAS  Google Scholar 

  69. Xiong J, He Z, Van Nostrand JD, Luo G, Tu S, Zhou J, Wang G (2012) Assessing the microbial community and functional genes in a vertical soil profile with long-term arsenic contamination. PLoS ONE 7:e50507–e50507. https://doi.org/10.1371/journal.pone.0050507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Jiang Y, Huang H, Tian Y, Yu X, Li X (2020) Stochasticity versus determinism: microbial community assembly patterns under specific conditions in petrochemical activated sludge. J Hazard Mater 407:124372. https://doi.org/10.1016/j.jhazmat.2020.124372

    Article  CAS  PubMed  Google Scholar 

  71. Xu R, Li B, Xiao E, Young LY, Sun X, Kong T, Dong Y, Wang Q, Yang Z, Chen L, Sun W (2020) Uncovering microbial responses to sharp geochemical gradients in a terrace contaminated by acid mine drainage. Environ Pollut 261:114226. https://doi.org/10.1016/j.envpol.2020.114226

    Article  CAS  PubMed  Google Scholar 

  72. Wang Z, Yuan S, Deng Z, Wang Y, Deng S, Song Y, Sun C, Bu N, Wang X (2020) Evaluating responses of nitrification and denitrification to the co-selective pressure of divalent zinc and tetracycline based on resistance genes changes. Bioresour Technol 314:123769. https://doi.org/10.1016/j.biortech.2020.123769

    Article  CAS  PubMed  Google Scholar 

  73. Fan MC, Guo YQ, Zhang LP, Zhu YM, Chen WM, Lin YB, Wei GH (2018) Herbaspirillum robiniae sp. nov., isolated from root nodules of Robinia pseudoacacia in a lead-zinc mine. Int J Syst Evol Microbiol 68:1300–1306. https://doi.org/10.1099/ijsem.0.002666

    Article  CAS  PubMed  Google Scholar 

  74. Di Gregorio S, Barbafieri M, Lampis S, Sanangelantoni AM, Tassi E, Vallini G (2006) Combined application of Triton X-100 and Sinorhizobium sp. Pb002 inoculum for the improvement of lead phytoextraction by Brassica juncea in EDTA amended soil. Chemosphere 63:293–299. https://doi.org/10.1016/j.chemosphere.2005.07.020

    Article  CAS  PubMed  Google Scholar 

  75. Liu H, Li P, Wang H, Qing C, Tan T, Shi B, Zhang G, Jiang Z, Wang Y, Hasan SZ (2020) Arsenic mobilization affected by extracellular polymeric substances (EPS) of the dissimilatory iron reducing bacteria isolated from high arsenic groundwater. Sci Total Environ 735:139501. https://doi.org/10.1016/j.scitotenv.2020.139501

    Article  CAS  PubMed  Google Scholar 

  76. Kou S, Vincent G, Gonzalez E, Pitre FE, Labrecque M, Brereton NJB (2018) The response of a 16S ribosomal RNA gene fragment amplified community to lead, zinc, and copper pollution in a Shanghai field trial. Front Microbiol 9:366. https://doi.org/10.3389/fmicb.2018.00366

    Article  PubMed  PubMed Central  Google Scholar 

  77. Montes-Grajales D, Esturau-Escofet N, Esquivel B, Martinez-Romero E (2019) Exo-metabolites of Phaseolus vulgaris-nodulating rhizobial strains. Metabolites 9:105. https://doi.org/10.3390/metabo9060105

    Article  CAS  PubMed Central  Google Scholar 

  78. Almon H, Böger P (1988) Hydrogen metabolism of the unicellular cyanobacterium Chroococcidiopsis thermalis ATCC29380. FEMS Microbiol Lett 49:445–449

    Article  CAS  Google Scholar 

  79. Aw E-E, Issa A (2000) Cyanobacteria as a biosorbent of heavy metals in sewage water. Environ Toxicol Pharmacol 8:95–101. https://doi.org/10.1016/S1382-6689(99)00037-X

    Article  Google Scholar 

  80. Brookes P (1995) The use of microbial parameters in monitoring soil pollution by heavy metals. Biol Fertil Soils 19:269–279. https://doi.org/10.1007/BF00336094

    Article  CAS  Google Scholar 

  81. Bertin PN, Heinrich-Salmeron A, Pelletier E, Goulhen-Chollet F, Arsène-Ploetze F, Gallien S, Lauga B, Casiot C, Calteau A, Vallenet D, Bonnefoy V, Bruneel O, Chane-Woon-Ming B, Cleiss-Arnold J, Duran R, Elbaz-Poulichet F, Fonknechten N, Giloteaux L, Halter D, Koechler S, Marchal M, Mornico D, Schaeffer C, Smith AAT, Van Dorsselaer A, Weissenbach J, Médigue C, Le Paslier D (2011) Metabolic diversity among main microorganisms inside an arsenic-rich ecosystem revealed by meta- and proteo-genomics. ISME J 5:1735–1747. https://doi.org/10.1038/ismej.2011.51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Li Y, Li Q, Chen S (2021) Diazotroph Paenibacillus triticisoli BJ-18 drives the variation in bacterial, diazotrophic and fungal communities in the rhizosphere and root/shoot endosphere of maize. Int J Mol Sci 22:1460. https://doi.org/10.3390/ijms22031460

  83. Xiao E, Ning Z, Xiao T, Sun W, Jiang S (2021) Soil bacterial community functions and distribution after mining disturbance. Soil Biol Biochem 157:108232. https://doi.org/10.1016/j.soilbio.2021.108232

    Article  CAS  Google Scholar 

  84. Li Y, Zhang M, Xu R, Lin H, Sun X, Xu F, Gao P, Kong T, Xiao E, Yang N, Sun W (2021) Arsenic and antimony co-contamination influences on soil microbial community composition and functions: relevance to arsenic resistance and carbon, nitrogen, and sulfur cycling. Environ Int 153:106522. https://doi.org/10.1016/j.envint.2021.106522

    Article  CAS  PubMed  Google Scholar 

  85. Park SC, Boyanov MI, Kemner KM, O’Loughlin EJ, Kwon MJ (2020) Distribution and speciation of Sb and toxic metal(loid)s near an antimony refinery and their effects on indigenous microorganisms. J Hazard Mater 403:123625. https://doi.org/10.1016/j.jhazmat.2020.123625

    Article  CAS  PubMed  Google Scholar 

  86. Zhu X, Yao J, Wang F, Yuan Z, Liu J, Jordan G, Knudsen T, Avdalović J (2018) Combined effects of antimony and sodium diethyldithiocarbamate on soil microbial activity and speciation change of heavy metals. Implications for contaminated lands hazardous material pollution in nonferrous metal mining areas. J Hazard Mater 349:160–167. https://doi.org/10.1016/j.jhazmat.2018.01.044

    Article  CAS  PubMed  Google Scholar 

  87. Xu R, Sun X, Lin H, Han F, Xiao E, Li B, Qiu L, Song B, Sun W (2020) Microbial adaptation in vertical soil profiles contaminated by antimony smelting plant. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiaa188

    Article  PubMed  Google Scholar 

  88. Cordero OX, Datta MS (2016) Microbial interactions and community assembly at microscales. Curr Opin Microbiol 31:227–234. https://doi.org/10.1016/j.mib.2016.03.015

    Article  PubMed  PubMed Central  Google Scholar 

  89. Kong T, Lin H, Xiao E, Xiao T, Gao P, Li B, Xu F, Qiu L, Wang X, Sun X, Sun W (2021) Investigation of the antimony fractions and indigenous microbiota in aerobic and anaerobic rice paddies. Sci Total Environ 771:145408. https://doi.org/10.1016/j.scitotenv.2021.145408

  90. Sun X, Xu R, Dong Y, Li F, Tao W, Kong T, Zhang M, Qiu L, Wang X, Sun W (2020) Investigation of the ecological roles of putative keystone taxa during tailing revegetation. Environ Sci Technol 54:11258–11270. https://doi.org/10.1021/acs.est.0c03031

    Article  CAS  PubMed  Google Scholar 

  91. Agler MT, Ruhe J, Kroll S, Morhenn C, Kim ST, Weigel D, Kemen EM (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol 14:e1002352. https://doi.org/10.1371/journal.pbio.1002352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Banerjee S, Schlaeppi K, van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576. https://doi.org/10.1038/s41579-018-0024-1

    Article  CAS  PubMed  Google Scholar 

  93. van der Heijden MG, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol 14:e1002378. https://doi.org/10.1371/journal.pbio.1002378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Dunne JA, Williams RJ, Martinez ND (2002) Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol Lett 5:558–567. https://doi.org/10.1046/j.1461-0248.2002.00354.x

    Article  Google Scholar 

  95. Masson-Boivin C, Sachs JL (2018) Symbiotic nitrogen fixation by rhizobia—the roots of a success story. Curr Opin Plant Biol 44:7–15. https://doi.org/10.1016/j.pbi.2017.12.001

    Article  CAS  PubMed  Google Scholar 

  96. Pajuelo E, Rodríguez-Llorente ID, Dary M, Palomares AJ (2008) Toxic effects of arsenic on Sinorhizobium-Medicago sativa symbiotic interaction. Environ Pollut 154:203–211. https://doi.org/10.1016/j.envpol.2007.10.015

    Article  CAS  PubMed  Google Scholar 

  97. Carrasco JA, Armario P, Pajuelo E, Burgos A, Caviedes MA, López R, Chamber MA, Palomares AJ (2005) Isolation and characterisation of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcóllar pyrite mine. Soil Biol Biochem 37:1131–1140. https://doi.org/10.1016/j.soilbio.2004.11.015

    Article  CAS  Google Scholar 

  98. Antoniadis V, Shaheen SM, Levizou E, Shahid M, Niazi NK, Vithanage M, Ok YS, Bolan N, Rinklebe J (2019) A critical prospective analysis of the potential toxicity of trace element regulation limits in soils worldwide: are they protective concerning health risk assessment? - A review. Environ Int 127:819–847. https://doi.org/10.1016/j.envint.2019.03.039

    Article  CAS  PubMed  Google Scholar 

  99. Ju W, Liu L, Jin X, Duan C, Cui Y, Wang J, Ma D, Zhao W, Wang Y, Fang L (2020) Co-inoculation effect of plant-growth-promoting rhizobacteria and rhizobium on EDDS assisted phytoremediation of Cu contaminated soils. Chemosphere 254:126724. https://doi.org/10.1016/j.chemosphere.2020.126724

    Article  CAS  PubMed  Google Scholar 

  100. Fan L-M, Ma Z-Q, Liang J-Q, Li H-F, Wang E-T, Wei G-H (2011) Characterization of a copper-resistant symbiotic bacterium isolated from Medicago lupulina growing in mine tailings. Biores Technol 102:703–709. https://doi.org/10.1016/j.biortech.2010.08.046

    Article  CAS  Google Scholar 

  101. Chen J, Liu YQ, Yan XW, Wei GH, Zhang JH, Fang LC (2018) Rhizobium inoculation enhances copper tolerance by affecting copper uptake and regulating the ascorbate-glutathione cycle and phytochelatin biosynthesis-related gene expression in Medicago sativa seedlings. Ecotoxicol Environ Saf 162:312–323. https://doi.org/10.1016/j.ecoenv.2018.07.001

    Article  CAS  PubMed  Google Scholar 

  102. Pajuelo E, Rodriguez-Llorente I, Lafuente A, Caviedes M (2011) Legume-rhizobium symbioses as a tool for bioremediation of heavy metal polluted soils. In: Khan, MS, Zaidi, A, Goel, R, Musarrat, J (eds) Biomanagement of Metal-Contaminated Soils. Springer, pp 95–123

  103. Wang Y, Wei D, Li P, Jiang Z, Liu H, Qing C, Wang H (2020) Diversity and arsenic-metabolizing gene clusters of indigenous arsenate-reducing bacteria in high arsenic groundwater of the Hetao Plain, Inner Mongolia. Ecotoxicology. https://doi.org/10.1007/s10646-020-02305-1

  104. Baldi F, Minacci A, Pepi M, Scozzafava A (2001) Gel sequestration of heavy metals by Klebsiella oxytoca isolated from iron mat. FEMS Microbiol Ecol 36:169–174

    Article  CAS  Google Scholar 

  105. Haq R, Zaidi SK, Shakoori A (1999) Cadmium resistant Enterobacter cloacae and Klebsiella sp. isolated from industrial effluents and their possible role in cadmium detoxification. World J Microbiol Biotechnol 15:283–290

    Article  Google Scholar 

  106. Sharma PK, Balkwill DL, Frenkel A, Vairavamurthy MA (2000) A new Klebsiella planticola strain (Cd-1) grows anaerobically at high cadmium concentrations and precipitates cadmium sulfide. Appl Environ Microbiol 66:3083–3087

    Article  CAS  Google Scholar 

  107. Mukherjee T, Banik A, Mukhopadhyay SK (2020) Plant growth-promoting traits of a thermophilic strain of the Klebsiella group with its effect on rice plant growth. Curr Microbiol 77:2613–2622. https://doi.org/10.1007/s00284-020-02032-0

    Article  CAS  PubMed  Google Scholar 

  108. Chakraborty A, Aziz Chowdhury A, Bhakat K, Islam E (2019) Elevated level of arsenic negatively influences nifH gene expression of isolated soil bacteria in culture condition as well as soil system. Environ Geochem Health 41:1953–1966. https://doi.org/10.1007/s10653-019-00261-2

    Article  CAS  PubMed  Google Scholar 

  109. Heimann K, Cirés S (2015) N2-fixing cyanobacteria: ecology and biotechnological applications. In: Kim S-K (ed) Handbook of Marine Microalgae. Elsevier, Academic Press, Boston, pp 501–515

    Chapter  Google Scholar 

  110. Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19:235–240

    Article  CAS  Google Scholar 

  111. Al-Homaidan AA, Alabdullatif JA, Al-Hazzani AA, Al-Ghanayem AA, Alabbad AF (2015) Adsorptive removal of cadmium ions by Spirulina platensis dry biomass. Saudi J Biol Sci 22:795–800. https://doi.org/10.1016/j.sjbs.2015.06.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Kwak HW, Kim MK, Lee JY, Yun H, Kim MH, Park YH, Lee KH (2015) Preparation of bead-type biosorbent from water-soluble Spirulina platensis extracts for chromium (VI) removal. Algal Res 7:92–99. https://doi.org/10.1016/j.algal.2014.12.006

    Article  Google Scholar 

  113. de Alvarenga LV, Lucius S, Vaz M, Araújo WL, Hagemann M (2020) The novel strain Desmonostoc salinum CCM-UFV059 shows higher salt and desiccation resistance compared to the model strain Nostoc sp. PCC7120. J Phycol 56:496–506. https://doi.org/10.1111/jpy.12968

    Article  CAS  PubMed  Google Scholar 

  114. Cui J, Xie Y, Sun T, Chen L, Zhang W (2020) Deciphering and engineering photosynthetic cyanobacteria for heavy metal bioremediation. Sci Total Environ 761:144111. https://doi.org/10.1016/j.scitotenv.2020.144111

    Article  CAS  PubMed  Google Scholar 

  115. Govarthanan M, Lee G-W, Park J-H, Kim JS, Lim S-S, Seo S-K, Cho M, Myung H, Kamala-Kannan S, Oh B-T (2014) Bioleaching characteristics, influencing factors of Cu solubilization and survival of Herbaspirillum sp. GW103 in Cu contaminated mine soil. Chemosphere 109:42–48. https://doi.org/10.1016/j.chemosphere.2014.02.054

    Article  CAS  PubMed  Google Scholar 

  116. Jiang Y, Zhang B, He C, Shi J, Borthwick AGL, Huang X (2018) Synchronous microbial vanadium (V) reduction and denitrification in groundwater using hydrogen as the sole electron donor. Water Res 141:289–296. https://doi.org/10.1016/j.watres.2018.05.033

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Caixia Wang for helping to improve the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (grant no. U20A20109), GDAS’ Project of Science and Technology Development (grant nos. 2020GDASYL-20200102015, 2021GDASYL-20210103048, 2020GDASYL-20200102014, 2021GDASYL-20210103041, 2019GDASYL-0103052, 2020GDASYL-20200103082, 2019GDASYL-0301002, and 2020GDASYL-20200402003); the Science and Technology Planning Project of Guangzhou (grant no. 202002020072, 201904010366); the High-Level Talents Project of the Pearl River Talents Recruitment Program (grant no. 2017GC010570); and the Local Innovative and Research Teams Project of Guangdong Pearl River Talents Program (grant no. 2017BT01Z176).

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Conceptualization: Weimin Sun, Yongbin Li; Methodology: Yongbin Li, Hanzhi Lin, Pin Gao, Nie Yang; Formal analysis and investigation: Yongbin Li, Hanzhi Lin, Rui Xu; Writing — original draft preparation: Xiaoxu Sun, Baoqin Li, Fuqing Xu, Xiaoyu Wang, Benru Song; Writing — review and editing: Weimin Sun, Yongbin Li, Hanzhi Lin; Funding acquisition: Weimin Sun; Supervision: Weimin Sun.

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Correspondence to Weimin Sun.

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Yongbin Li and Hanzhi Lin contributed equally to this work.

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Li, Y., Lin, H., Gao, P. et al. Synergistic Impacts of Arsenic and Antimony Co-contamination on Diazotrophic Communities. Microb Ecol 84, 44–58 (2022). https://doi.org/10.1007/s00248-021-01824-6

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