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
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
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
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
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
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
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
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
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
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
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
Sundar S, Chakravarty J (2010) Antimony toxicity. Int J Environ Res Public Health 7:4267–4277. https://doi.org/10.3390/ijerph7124267
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Pau R (1989) Nitrogenase without molybdenum. Trends Biochem Sci 14:183–186. https://doi.org/10.1016/0968-0004(89)90271-5
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
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
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
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
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
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
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
Glick B (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. https://doi.org/10.1016/j.biotechadv.2010.02.001
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Csardi G, Nepusz T (2005) The igraph software package for complex network research. Inter J Complex Syst 1695, 1–9
Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci 103:8577. https://doi.org/10.1073/pnas.0601602103
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
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
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
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
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
Matthews JA (1992) The ecology of recently-deglaciated terrain: a geoecological approach to glacier forelands. Cambridge University Press, Cambridge, UK
Walker LR, Del Moral R (2003) Primary succession and ecosystem rehabilitation. Cambridge University Press, Cambridge
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
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
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
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
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
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
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
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
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
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
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
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
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
Almon H, Böger P (1988) Hydrogen metabolism of the unicellular cyanobacterium Chroococcidiopsis thermalis ATCC29380. FEMS Microbiol Lett 49:445–449
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
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
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
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
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
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
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
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
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
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
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
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
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
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
van der Heijden MG, Hartmann M (2016) Networking in the plant microbiome. PLoS Biol 14:e1002378. https://doi.org/10.1371/journal.pbio.1002378
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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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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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DOI: https://doi.org/10.1007/s00248-021-01824-6