Skip to main content

Advertisement

Log in

Patterns of Bacterial Diversity Along a Long-Term Mercury-Contaminated Gradient in the Paddy Soils

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Mercury (Hg) pollution is usually regarded as an environmental stress in reducing microbial diversity and altering bacterial community structure. However, these results were based on relatively short-term studies, which might obscure the real response of microbial species to Hg contamination. Here, we analysed the bacterial abundance and community composition in paddy soils that have been potentially contaminated by Hg for more than 600 years. Expectedly, the soil Hg pollution significantly influenced the bacterial community structure. However, the bacterial abundance was significantly correlated with the soil organic matter content rather than the total Hg (THg) concentration. The bacterial alpha diversity increased at relatively low levels of THg and methylmercury (MeHg) and subsequently approached a plateau above 4.86 mg kg−1 THg or 18.62 ng g−1 MeHg, respectively. Contrasting with the general prediction of decreasing diversity along Hg stress, our results seem to be consistent with the intermediate disturbance hypotheses with the peak biological diversity under intermediate disturbance or stress. This result was partly supported by the inconsistent response of bacterial species to Hg stress. For instance, the relative abundance of Nitrospirae decreased, while that of Gemmatimonadetes increased significantly along the increasing soil THg and MeHg concentrations. In addition, the content of SO4 2−, THg, MeHg and soil depth were the four main factors influencing bacterial community structures based on the canonical correspondence analysis (CCA). Overall, our findings provide novel insight into the distribution patterns of bacterial community along the long-term Hg-contaminated gradient in paddy soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Krabbenhoft DP, Sunderland EM (2013) Global change and mercury. Science 341:1457–1458

    Article  CAS  PubMed  Google Scholar 

  2. McNutt M (2013) Mercury and health. Science 341:1430

    Article  CAS  PubMed  Google Scholar 

  3. Tchounwou PB, Ayensu WK, Ninashvili N, Sutton D (2003) Environmental exposure to mercury and its toxicopathologic implications for public health. Environ Toxicol 18:149–175

    Article  CAS  PubMed  Google Scholar 

  4. Rasmussen LD, Sorensen SJ (2001) Effects of mercury contamination on the culturable heterotrophic, functional and genetic diversity of the bacterial community in soil. FEMS Microbiol Ecol 36:1–9

    Article  CAS  PubMed  Google Scholar 

  5. Muller AK, Westergaard K, Christensen S, Sorensen SJ (2001) The effect of long-term mercury pollution on the soil microbial community. FEMS Microbiol Ecol 36:11–19

    Article  CAS  PubMed  Google Scholar 

  6. Harris-Hellal J, Vallaeys T, Garnier-Zarli E, Bousserrhine N (2009) Effects of mercury on soil microbial communities in tropical soils of French Guyana. Appl Soil Ecol 41:59–68

    Article  Google Scholar 

  7. Frey B, Rieder SR (2013) Response of forest soil bacterial communities to mercury chloride application. Soil Biol Biochem 65:329–337

    Article  CAS  Google Scholar 

  8. Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73:395–415

    Article  CAS  Google Scholar 

  9. Muller AK, Westergaard K, Christensen S, Sorensen SJ (2002) The diversity and function of soil microbial communities exposed to different disturbances. Microb Ecol 44:49–58

    Article  CAS  PubMed  Google Scholar 

  10. Maliszewska W, Dec S, Wierzbicka H, Wozniakowska A (1985) The influence of various heavy metal compounds on the development and activity of soil microorganisms. Environ Pollut 37:195–215

    Article  CAS  Google Scholar 

  11. Casucci C, Okeke BC, Frankenberger WT (2002) Effects of mercury on microbial biomass and enzyme activities in soil. Biol Trace Elem Res 94:179–191

    Article  Google Scholar 

  12. Liu YR, Zheng YM, Shen JP, Zhang LM, He JZ (2010) Effects of mercury on the activity and community composition of soil ammonia oxidizers. Environ Sci Pollut Res 17:1237–1244

    Article  CAS  Google Scholar 

  13. Hartmann M, Niklaus PA, Zimmermann S, Schmutz S, Kremer J, Abarenkov K, Lüscher P, Widmer F, Frey B (2014) Resistance and resilience of the forest soil microbiome to logging-associated compaction. ISME J 8:226–244

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Singh BK, Quince C, Macdonald CA, Khachane A, Thomas N, Al-Soud WA, Sørensen SJ, He Z, White D, Sinclair A, Crooks B, Zhou J, Campbell CD (2014) Loss of microbial diversity in soils is coincident with reductions in some specialized functions. Environ Microbiol. doi:10.1111/1462-2920.12353

    Google Scholar 

  15. Liu YR, Zheng YM, Zhang LM, He JZ (2014) Linkage between community diversity of sulfate-reducing microorganisms and methylmercury concentration in paddy soil. Environ Sci Pollut Res 21:1339–1348

    Article  CAS  Google Scholar 

  16. Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384

    Article  CAS  PubMed  Google Scholar 

  17. Chadhain SMN, Schaefer JK, Crane S, Zylstra GJ, Barkay T (2006) Analysis of mercuric reductase (merA) gene diversity in an anaerobic mercury-contaminated sediment enrichment. Environ Microbiol 8:1746–1752

    Article  CAS  Google Scholar 

  18. Parks JM, Johs A, Podar M, Bridou R, Hurt RA, Smith SD, Tomanicek SJ, Qian Y, Brown SD, Brandt CC, Palumbo AV, Smith JC, Wall JD, Elias DA, Liang L (2013) The genetic basis for bacterial mercury methylation. Science 339:1332–1335

    Article  CAS  PubMed  Google Scholar 

  19. Liu YR, Yu RQ, Zheng YM, He JZ (2014) Analysis of community structure of Hg methylation gene (hgcA) in paddy soils along an Hg gradient. Appl Environ Microbiol. doi:10.1128/AEM.04225-13

    Google Scholar 

  20. Gilmour CC, Henry EA, Mitchell R (1992) Sulfate-stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281–2287

    Article  CAS  Google Scholar 

  21. Yu RQ, Adatto I, Montesdeoca MR, Driscoll CT, Hines ME, Barkay T (2010) Mercury methylation in Sphagnum moss mats and its association with sulfate -reducing bacteria in an acidic Adirondack forest lake wetland. FEMS Microbiol Ecol 74:655–668

    Article  CAS  PubMed  Google Scholar 

  22. Fleming EJ, Mack EE, Green PG, Nelson DC (2006) Mercury methylation from unexpected sources: molybdate-inhibited freshwater sediments and an iron-reducing bacterium. Appl Environ Microbiol 72:457–464

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Yu RQ, Flanders JR, Mack EE, Turner R, Mirza MB, Barkay T (2012) Contribution of coexisting sulfate and iron reducing bacteria to methylmercury production in freshwater river sediments. Environ Sci Technol 46:2684–2691

    Article  CAS  PubMed  Google Scholar 

  24. Yu RQ, Reinfelder JR, Hines ME, Barkay T (2013) Mercury methylation by the methanogen Methanospirillum hungatei. Appl Environ Microbiol 79:6325–6330

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Gilmour CC, Podar M, Bullock AL, Graham AM, Brown S, Somenahally AC, Johs A, Hurt R, Bailey KL, Elias D (2013) Mercury methylation by novel microorganisms from new environments. Environ Sci Technol 47:11810–11820

    Article  CAS  PubMed  Google Scholar 

  26. Vishnivetskaya TA, Mosher JJ, Palumbo AV, Yang ZK, Podar M, Brown SD, Brook SC, Gu, Southworth GR, Drake MM, Brandt CC, Elias DA (2011) Mercury and Other Heavy metals influence bacterial community structure in contaminated Tennessee streams. Appl Environ Microbiol 77:302–311

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Feng X, Li P, Qiu G, Wang S, Li G, Shang L, Meng B, Jiang H, Bai W, Li Z, Fu X (2008) Human exposure to methylmercury through rice intake in mercury mining areas, Guizhou province, China. Environ Sci Technol 42:326–332

    Article  CAS  PubMed  Google Scholar 

  28. Zhang H, Feng XB, Larssen T, Shang L, Li P (2010) Bioaccumulation of methylmercury versus inorganic mercury in rice (Oryza sativa L.) grain. Environ Sci Technol 44:4499–4504

    Article  CAS  PubMed  Google Scholar 

  29. Li P, Feng X, Yuan X, Chan HM, Qiu G, Sun GX, Zhu YG (2012) Rice consumption contributes to low level methylmercury exposure in southern China. Environ Int 9:18–23

    Article  CAS  Google Scholar 

  30. Rothenberg SE, Feng XB (2012) Mercury cycling in a flooded rice paddy. J Geophys Res 117, G03003

    Google Scholar 

  31. Downing AL, Leibold MA (2002) Ecosystem consequences of species richness and composition in pond food webs. Nature 416:837–841

    Article  CAS  PubMed  Google Scholar 

  32. Chen D, Jing M, Wang X (2005) Determination of methyl mercury in water and soil by HPLC–ICP-MS, Agilent Technologies. 8

  33. Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Suzuki MT, Taylor LT, Delong EF (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 50-nuclease assays. Appl Environ Microbiol 66:4605–4614

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  38. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G et al (2011) Chimeric 16S rRNAsequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21:494–504

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K et al (2006) Greengenes, a chimera checked 16S rRNA gene database and work bench compatible with ARB. Appl Environ Microbiol 72:5069–5072

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Connell JH (1979) Intermediate-disturbance hypothesis. Science 204:1345

    Article  CAS  PubMed  Google Scholar 

  41. Odum EP (1981) The effects of stress on the trajectory of ecological succession. In: Barrett GW, Rosenburg R (eds) Stress effects on natural ecosystems. Wiley, London, pp 43–47

    Google Scholar 

  42. Broos K, Mertens J, Smolders E (2005) Toxicity of heavy metals in soil assessed with various soil microbial and plant growth assays: a comparative study. Environ Toxicol Chem 24:634–640

    Article  CAS  PubMed  Google Scholar 

  43. Giller KE, Witter E, McGrath SP (1998) Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:1389–1414

    Article  CAS  Google Scholar 

  44. Taylor JP, Wilson B, Mills MS, Burns RG (2002) Comparison of microbial numbers and enzymatic activities in surface soils and subsoils using various techniques. Soil Biol Biochem 34:387–401

    Article  CAS  Google Scholar 

  45. Schultz P, Urban NR (2008) Effects of bacterial dynamics on organic matter decomposition and nutrient release from sediments: a modeling study. Ecol Model 210:1–14

    Article  CAS  Google Scholar 

  46. Khwaja AR, Bloom PR, Brezonik PL (2010) Binding strength of methylmercury to aquatic NOM. Environ Sci Technol 44:6151–6156

    Article  CAS  PubMed  Google Scholar 

  47. Rieder SR, Frey B (2013) Methyl-mercury affects microbial activity and biomass, bacterial community structure but rarely the fungal community structure. Soil Biol Biochem 64:164–173

    Article  CAS  Google Scholar 

  48. Sullivan TS, McBride MB, Thies JE (2013) Rhizosphere microbial community and Zn uptake by willow (Salix purpurea L.) depend on soil sulfur concentrations in metalliferous peat soils. Appl Soil Ecol 67:53–60

    Article  Google Scholar 

  49. Eilers KG, Debenport S, Anderson S, Fierer N (2012) Digging deeper to find unique microbial communities: the strong effect of depth on the structure of bacterial and archaeal communities in soil. Soil Biol Biochem 50:58–65

    Article  CAS  Google Scholar 

  50. Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715

    Article  PubMed  Google Scholar 

  51. Shrestha PM, Kube M, Reinhardt R, Liesack W (2009) Transcriptional activity of paddy soil bacterial communities. Environ Microbiol 11:960–970

    Article  CAS  PubMed  Google Scholar 

  52. Ahn JH, Song J, Kim BY, Kim MS, Joa JH, Weon HY (2012) Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices. J Microbiol 50:754–765

    Article  PubMed  Google Scholar 

  53. Das S, Jean JS, Kar S, Liu CC (2013) Changes in bacterial community structure and abundance in agricultural soils under varying levels of arsenic contamination. Geomicrobiol J 30:635–644

    Article  CAS  Google Scholar 

  54. Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390

    Article  CAS  PubMed  Google Scholar 

  55. Oregaard G, Sorensen SJ (2007) High diversity of bacterial mercuric reductase genes from surface and sub-surface floodplain soil (Oak Ridge, USA). ISME J 1:453–467

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (41201523 and 41025004). We would like to thank Mr. Xing-Wang Shi for his assistance in soil sampling. We are also grateful to Jun-Tao Wang for his assistance in the data analysis.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ji-Zheng He.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table S1

(DOCX 29 kb)

Figure S1

Regressions between abundance of 16S rRNA gene sequences and methylmercury (MeHg) content. (DOCX 37 kb)

Figure S2

The relative abundance of bacterial class along the increasing total Hg (THg) and (MeHg) concentrations. (DOCX 63 kb)

Figure S3

The relative abundance of bacterial order along the increasing THg concentration. (DOCX 62 kb)

Figure S4

The relative abundance of bacterial order along the increasing (MeHg) concentration. (DOCX 47 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, YR., Wang, JJ., Zheng, YM. et al. Patterns of Bacterial Diversity Along a Long-Term Mercury-Contaminated Gradient in the Paddy Soils. Microb Ecol 68, 575–583 (2014). https://doi.org/10.1007/s00248-014-0430-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0430-5

Keywords

Navigation