Short-Term Legacy Effects of Mercury Contamination on Plant Growth and nifH-Harboring Microbial Community in Rice Paddy Soil

Abstract

Methylmercury (MeHg), which is formed in rice paddy soil, exhibits strong neurotoxicity through bioaccumulation in the food chain. A few groups of microorganisms drive both mercury methylation and nitrogen fixation in the rhizosphere. Little is known about how the shifted soil microbial community by Hg contamination affects nitrogen fixation rate and plant growth in paddy soil. Here, we examined how stimulated short-term Hg amendment affects the nitrogen fixing microbial community and influences plant-microbe interactions. Soil was treated with low (0.2 mg/kg) and high (1.1 mg/kg) concentrations of Hg for 4 weeks; then, rice (Oryza sativa) was planted and grown for 12 weeks. The nitrogen-fixation rate and rice growth were measured. The diversity and structure of the microbial community were analyzed by sequencing the nifH gene before and after rice cultivation. Hg treatments significantly decreased the nitrogen fixation rate and dry weight of the rice plants. The structure of the nifH-harboring community was remarkably changed after rice cultivation depending on Hg treatments. Iron- or sulfate-reducing bacteria, including Desulfobacca, Desulfoporosimus, and Geobacter, were observed as legacy response groups; their abundances increased in the soil after Hg treatment. The high abundance of those groups were maintained in control, but the abundance drastically decreased after rice cultivation in the soil treated with Hg, indicating that symbiotic behavior of rice plants changes according to the legacy effects on Hg contamination. These results suggested that Hg contamination can persist in soil microbial communities, affecting their nitrogen-fixation ability and symbiosis with rice plants in paddy soil.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Data Availability

All data generated or analyzed during this study are included in this published article and its supplementary information files. The raw sequence data have been deposited in the NCBI BioProject repository, https://www.ncbi.nlm.nih.gov/bioproject/PRJNA640989.

References

  1. 1.

    Ha E, Basu N, Bose-O'Reilly S, Dorea JG, McSorley E, Sakamoto M, Chan HM (2017) Current progress on understanding the impact of mercury on human health. Environ Res 152:419–433. https://doi.org/10.1016/j.envres.2016.06.042

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983. https://doi.org/10.1021/es305071v

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Liu YR, Johs A, Bi L, Lu X, Hu HW, Sun D, He JZ, Gu B (2018) Unraveling microbial communities associated with methylmercury production in paddy soils. Environ Sci Technol 52:13110–13118. https://doi.org/10.1021/acs.est.8b03052

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Liu J, Wang J, Ning Y, Yang S, Wang P, Shaheen SM, Feng X, Rinklebe J (2019) Methylmercury production in a paddy soil and its uptake by rice plants as affected by different geochemical mercury pools. Environ Int 129:461–469. https://doi.org/10.1016/j.envint.2019.04.068

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Regnell O, Watras CJ (2019) Microbial mercury methylation in aquatic environments: a critical review of published field and laboratory studies. Environ Sci Technol 53:4–19. https://doi.org/10.1021/acs.est.8b02709

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Liu M, Zhang Q, Cheng M, He Y, Chen L, Zhang H, Cao H, Shen H, Zhang W, Tao S, Wang X (2019) Rice life cycle-based global mercury biotransport and human methylmercury exposure. Nat Commun 10:5164. https://doi.org/10.1038/s41467-019-13221-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Tang WL, Liu YR, Guan WY, Zhong H, Qu XM, Zhang T (2020) Understanding mercury methylation in the changing environment: recent advances in assessing microbial methylators and mercury bioavailability. Sci Total Environ 714:136827. https://doi.org/10.1016/j.scitotenv.2020.136827

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Zhao L, Qiu G, Anderson CWN, Meng B, Wang D, Shang L, Yan H, Feng X (2016) Mercury methylation in rice paddies and its possible controlling factors in the Hg mining area, Guizhou province, Southwest China. Environ Pollut 215:1–9. https://doi.org/10.1016/j.envpol.2016.05.001

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Wang H, Guo CL, Yang CF, Lu GN, Chen MQ, Dang Z (2016) Distribution and diversity of bacterial communities and sulphate-reducing bacteria in a paddy soil irrigated with acid mine drainage. J Appl Microbiol 121:196–206. https://doi.org/10.1111/jam.13143

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Liu H, Brettell LE, Qiu Z, Singh BK (2020) Microbiome-Mediated Stress Resistance in Plants. Trends Plant Sci 25:733–743. https://doi.org/10.1016/j.tplants.2020.03.014

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Gilmour CC, Podar M, Bullock AL, Graham AM, Brown SD, Somenahally AC, Johs A, Hurt Jr RA, Bailey KL, Elias DA (2013) Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810–11820. https://doi.org/10.1021/es403075t

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Masuda Y, Itoh H, Shiratori Y, Isobe K, Otsuka S, Senoo K (2017) Predominant but Previously-overlooked Prokaryotic Drivers of Reductive Nitrogen Transformation in Paddy Soils, Revealed by Metatranscriptomics. Microbes Environ 32:180–183. https://doi.org/10.1264/jsme2.ME16179

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Li L, Jia R, Qu Z, Li T, Shen W, Qu D (2020) Coupling between nitrogen-fixing and iron(III)-reducing bacteria as revealed by the metabolically active bacterial community in flooded paddy soils amended with glucose. Sci Total Environ 716:137056. https://doi.org/10.1016/j.scitotenv.2020.137056

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AM, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45. https://doi.org/10.1038/ngeo366

    CAS  Article  Google Scholar 

  15. 15.

    Goni-Urriza M, Corsellis Y, Lanceleur L, Tessier E, Gury J, Monperrus M, Guyoneaud R (2015) Relationships between bacterial energetic metabolism, mercury methylation potential, and hgcA/hgcB gene expression in Desulfovibrio dechloroacetivorans BerOc1. Environ Sci Pollut Res Int 22:13764–13771. https://doi.org/10.1007/s11356-015-4273-5

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Jean-Philippe SR, Franklin JA, Buckley DS, Hughes K (2011) The effect of mercury on trees and their mycorrhizal fungi. Environ Pollut 159:2733–2739. https://doi.org/10.1016/j.envpol.2011.05.017

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Azevedo R, Rodriguez E (2012) Phytotoxicity of mercury in plants: a review. J Bot 2012:848614–848616. https://doi.org/10.1155/2012/848614

    CAS  Article  Google Scholar 

  18. 18.

    Souza R, Ambrosini A, Passaglia LM (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38:401–419. https://doi.org/10.1590/S1415-475738420150053

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Li X, Zhang J, Gong Y, Yang S, Ye M, Yu X, Ma J (2020) Status of mercury accumulation in agricultural soils across China (1976-2016). Ecotoxicol Environ Saf 197:110564. https://doi.org/10.1016/j.ecoenv.2020.110564

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    AGENCY. UEP (1998) Mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrophotometry. Method 7473. US Environmental Protection Agency Washington, DC

  21. 21.

    EPA (2001) Method 1630: Methyl Mercury in Water by Distillation, Aqueous Ethylation, Purge and Trap, and CVAFS (EPA-821-R-01-020, January 2001). Office of Water, Office of Science and Technology, Engineering and Analysis ….

  22. 22.

    Hugerth LW, Andersson AF (2017) Analysing microbial community composition through amplicon sequencing: from sampling to hypothesis testing. Front Microbiol 8:1561. https://doi.org/10.3389/fmicb.2017.01561

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Messer LF, Mahaffey C, Robinson CM, Jeffries TC, Baker KG, Bibiloni Isaksson J, Ostrowski M, Doblin MA, Brown MV, Seymour JR (2016) High levels of heterogeneity in diazotroph diversity and activity within a putative hotspot for marine nitrogen fixation. ISME J 10:1499–1513. https://doi.org/10.1038/ismej.2015.205

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Bravo AG, Zopfi J, Buck M, Xu J, Bertilsson S, Schaefer JK, Pote J, Cosio C (2018) Geobacteraceae are important members of mercury-methylating microbial communities of sediments impacted by waste water releases. ISME J 12:802–812. https://doi.org/10.1038/s41396-017-0007-7

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Sorkhoh NA, Ali N, Dashti N, Al-Mailem DM, Al-Awadhi H, Eliyas M, Radwan SS (2010) Soil bacteria with the combined potential for oil utilization, nitrogen fixation, and mercury resistance. Int Biodeterior Biodegradation 64:226–231. https://doi.org/10.1016/j.ibiod.2009.10.011

    CAS  Article  Google Scholar 

  26. 26.

    Zeyaullah M, Islam B, Ali A (2010) Isolation, identification and PCR amplification of merA gene from highly mercury polluted Yamuna river. Afr J Biotechnol 9:3510–3514

    CAS  Google Scholar 

  27. 27.

    Figueiredo N, Serralheiro ML, Canario J, Duarte A, Hintelmann H, Carvalho C (2018) Evidence of mercury methylation and demethylation by the estuarine microbial communities obtained in stable hg isotope studies. Int J Environ Res Public Health 15. https://doi.org/10.3390/ijerph15102141

  28. 28.

    Bissett A, Brown MV, Siciliano SD, Thrall PH (2013) Microbial community responses to anthropogenically induced environmental change: towards a systems approach. Ecol Lett 16(Suppl 1):128–139. https://doi.org/10.1111/ele.12109

    Article  PubMed  Google Scholar 

  29. 29.

    Wang L, Wang LA, Zhan X, Huang Y, Wang J, Wang X (2020) Response mechanism of microbial community to the environmental stress caused by the different mercury concentration in soils. Ecotoxicol Environ Saf 188:109906. https://doi.org/10.1016/j.ecoenv.2019.109906

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Zhang H, Feng X, Zhu J, Sapkota A, Meng B, Yao H, Qin H, Larssen T (2012) Selenium in soil inhibits mercury uptake and translocation in rice (Oryza sativa L.). Environ Sci Technol 46:10040–10046. https://doi.org/10.1021/es302245r

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Gontia-Mishra I, Sapre S, Sharma A, Tiwari S (2016) Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. J Plant Growth Regul 35:1000–1012. https://doi.org/10.1007/s00344-016-9598-x

    CAS  Article  Google Scholar 

  32. 32.

    Mus F, Crook MB, Garcia K, Garcia Costas A, Geddes BA, Kouri ED, Paramasivan P, Ryu MH, Oldroyd GED, Poole PS, Udvardi MK, Voigt CA, Ane JM, Peters JW (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710. https://doi.org/10.1128/AEM.01055-16

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Ma M, Du H, Wang D (2019) Mercury methylation by anaerobic microorganisms: A review. Crit Rev Environ Sci Technol 49:1893–1936. https://doi.org/10.1080/10643389.2019.1594517

    CAS  Article  Google Scholar 

  34. 34.

    Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Doornbos RF, van Loon LC, Bakker PA (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243. https://doi.org/10.1007/s13593-011-0028-y

    Article  Google Scholar 

  36. 36.

    Podar M, Gilmour CC, Brandt CC, Soren A, Brown SD, Crable BR, Palumbo AV, Somenahally AC, Elias DA (2015) Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci Adv 1:e1500675. https://doi.org/10.1126/sciadv.1500675

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Vishnivetskaya TA, Hu H, Van Nostrand JD, Wymore AM, Xu X, Qiu G, Feng X, Zhou J, Brown SD, Brandt CC, Podar M, Gu B, Elias DA (2018) Microbial community structure with trends in methylation gene diversity and abundance in mercury-contaminated rice paddy soils in Guizhou, China. Environ Sci Process Impacts 20:673–685. https://doi.org/10.1039/c7em00558j

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Xu J, Buck M, Eklof K, Ahmed OO, Schaefer JK, Bishop K, Skyllberg U, Bjorn E, Bertilsson S, Bravo AG (2019) Mercury methylating microbial communities of boreal forest soils. Sci Rep 9:518. https://doi.org/10.1038/s41598-018-37383-z

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Breidenbach B, Pump J, Dumont MG (2015) Microbial community structure in the rhizosphere of rice plants. Front Microbiol 6:1537. https://doi.org/10.3389/fmicb.2015.01537

    Article  PubMed  Google Scholar 

  40. 40.

    Edwards J, Santos-Medellin C, Nguyen B, Kilmer J, Liechty Z, Veliz E, Ni J, Phillips G, Sundaresan V (2019) Soil domestication by rice cultivation results in plant-soil feedback through shifts in soil microbiota. Genome Biol 20:221. https://doi.org/10.1186/s13059-019-1825-x

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Cuddington K (2011) Legacy effects: the persistent impact of ecological interactions. Biol Theory 6:203–210. https://doi.org/10.1007/s13752-012-0027-5

    Article  Google Scholar 

  42. 42.

    Jurburg SD, Nunes I, Brejnrod A, Jacquiod S, Prieme A, Sorensen SJ, Van Elsas JD, Salles JF (2017) Legacy effects on the recovery of soil bacterial communities from extreme temperature perturbation. Front Microbiol 8:1832. https://doi.org/10.3389/fmicb.2017.01832

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Li X, Jousset A, de Boer W, Carrión VJ, Zhang T, Wang X, Kuramae EE (2019) Legacy of land use history determines reprogramming of plant physiology by soil microbiome. ISME J 13:738–751. https://doi.org/10.1038/s41396-018-0300-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Wang X, Ye Z, Li B, Huang L, Meng M, Shi J, Jiang G (2014) Growing rice aerobically markedly decreases mercury accumulation by reducing both Hg bioavailability and the production of MeHg. Environ Sci Technol 48:1878–1885. https://doi.org/10.1021/es4038929

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Hu Y, Cheng H, Tao S (2018) The growing importance of waste-to-energy (WTE) incineration in China's anthropogenic mercury emissions: Emission inventories and reduction strategies. Renew Sust Energ Rev 97:119–137. https://doi.org/10.1016/j.rser.2018.08.026

    CAS  Article  Google Scholar 

  46. 46.

    Cordovez V, Dini-Andreote F, Carrión VJ, Raaijmakers JM (2019) Ecology and Evolution of Plant Microbiomes. Annu Rev Microbiol 73:69–88. https://doi.org/10.1146/annurev-micro-090817-062524

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Wang Y, Dang F, Zhong H, Wei Z, Li P (2016) Effects of sulfate and selenite on mercury methylation in a mercury-contaminated rice paddy soil under anoxic conditions. Environ Sci Pollut Res Int 23:4602–4608. https://doi.org/10.1007/s11356-015-5696-8

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Chen J, Li JM, Tang YJ, Xing YM, Qiao P, Li Y, Liu PG, Guo SX (2019) Chinese black truffle-associated bacterial communities of tuber indicum from different geographical regions with nitrogen fixing bioactivity. Front Microbiol 10:2515. https://doi.org/10.3389/fmicb.2019.02515

    Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Han L-L, Wang Q, Shen J-P, Di HJ, Wang J-T, Wei W-X, Fang Y-T, Zhang L-M, He J-Z (2019) Multiple factors drive the abundance and diversity of the diazotrophic community in typical farmland soils of China. FEMS Microbiol Ecol 95:fiz113. https://doi.org/10.1093/femsec/fiz113

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Hoon Je Seong at Chun-Ang University for providing processing sequence data and community analysis.

Funding

This work supported by a grant from Strategic Initiative for Microbiomes in Agriculture and Food, Ministry of Agriculture, Food and Rural Affairs (Project No. 918014-4) and Korea Ministry of Environment as Subsurface Environment Management Projects (No. 2020002480003).

Author information

Affiliations

Authors

Contributions

Hye Rim Hyun performed data analysis and wrote the manuscript; Eun Sun Lyu, Jin Ju Kim and Hakwon Yoon assisted with designing the analysis and revising the manuscript. Sae Yun Kwon and Tae Kwon Lee designed and coordinated the project, performed data analysis, and revised the manuscript.

Corresponding author

Correspondence to Tae Kwon Lee.

Ethics declarations

Conflict of Interest

The authors declare they have no competing interests.

Supplementary Information

ESM 1

(DOCX 158 kb).

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hyun, H.R., Yoon, H., Lyou, E.S. et al. Short-Term Legacy Effects of Mercury Contamination on Plant Growth and nifH-Harboring Microbial Community in Rice Paddy Soil. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01722-x

Download citation

Keywords

  • Paddy soil
  • Nitrogen fixation
  • Mercury methylation
  • Microbial community