Microbial Ecology

, Volume 68, Issue 3, pp 575–583 | Cite as

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

  • Yu-Rong Liu
  • Jian-Jun Wang
  • Yuan-Ming Zheng
  • Li-Mei Zhang
  • Ji-Zheng He
Soil Microbiology

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 SO42−, 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.

Supplementary material

248_2014_430_MOESM1_ESM.docx (29 kb)
Table S1(DOCX 29 kb)
248_2014_430_MOESM2_ESM.docx (37 kb)
Figure S1Regressions between abundance of 16S rRNA gene sequences and methylmercury (MeHg) content. (DOCX 37 kb)
248_2014_430_MOESM3_ESM.docx (64 kb)
Figure S2The relative abundance of bacterial class along the increasing total Hg (THg) and (MeHg) concentrations. (DOCX 63 kb)
248_2014_430_MOESM4_ESM.docx (63 kb)
Figure S3The relative abundance of bacterial order along the increasing THg concentration. (DOCX 62 kb)
248_2014_430_MOESM5_ESM.docx (48 kb)
Figure S4The relative abundance of bacterial order along the increasing (MeHg) concentration. (DOCX 47 kb)

References

  1. 1.
    Krabbenhoft DP, Sunderland EM (2013) Global change and mercury. Science 341:1457–1458CrossRefPubMedGoogle Scholar
  2. 2.
    McNutt M (2013) Mercury and health. Science 341:1430CrossRefPubMedGoogle Scholar
  3. 3.
    Tchounwou PB, Ayensu WK, Ninashvili N, Sutton D (2003) Environmental exposure to mercury and its toxicopathologic implications for public health. Environ Toxicol 18:149–175CrossRefPubMedGoogle Scholar
  4. 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 36:1–9CrossRefPubMedGoogle Scholar
  5. 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 36:11–19CrossRefPubMedGoogle Scholar
  6. 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 41:59–68CrossRefGoogle Scholar
  7. 7.
    Frey B, Rieder SR (2013) Response of forest soil bacterial communities to mercury chloride application. Soil Biol Biochem 65:329–337CrossRefGoogle Scholar
  8. 8.
    Balser TC, Firestone MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73:395–415CrossRefGoogle Scholar
  9. 9.
    Muller AK, Westergaard K, Christensen S, Sorensen SJ (2002) The diversity and function of soil microbial communities exposed to different disturbances. Microb Ecol 44:49–58CrossRefPubMedGoogle Scholar
  10. 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 37:195–215CrossRefGoogle Scholar
  11. 11.
    Casucci C, Okeke BC, Frankenberger WT (2002) Effects of mercury on microbial biomass and enzyme activities in soil. Biol Trace Elem Res 94:179–191CrossRefGoogle Scholar
  12. 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 17:1237–1244CrossRefGoogle Scholar
  13. 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 8:226–244PubMedCentralCrossRefPubMedGoogle Scholar
  14. 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. 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 21:1339–1348CrossRefGoogle Scholar
  16. 16.
    Barkay T, Miller SM, Summers AO (2003) Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Rev 27:355–384CrossRefPubMedGoogle Scholar
  17. 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 8:1746–1752CrossRefGoogle Scholar
  18. 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 339:1332–1335CrossRefPubMedGoogle Scholar
  19. 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. 20.
    Gilmour CC, Henry EA, Mitchell R (1992) Sulfate-stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281–2287CrossRefGoogle Scholar
  21. 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 74:655–668CrossRefPubMedGoogle Scholar
  22. 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 72:457–464PubMedCentralCrossRefPubMedGoogle Scholar
  23. 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 46:2684–2691CrossRefPubMedGoogle Scholar
  24. 24.
    Yu RQ, Reinfelder JR, Hines ME, Barkay T (2013) Mercury methylation by the methanogen Methanospirillum hungatei. Appl Environ Microbiol 79:6325–6330PubMedCentralCrossRefPubMedGoogle Scholar
  25. 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 47:11810–11820CrossRefPubMedGoogle Scholar
  26. 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 77:302–311PubMedCentralCrossRefPubMedGoogle Scholar
  27. 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 42:326–332CrossRefPubMedGoogle Scholar
  28. 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 44:4499–4504CrossRefPubMedGoogle Scholar
  29. 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 9:18–23CrossRefGoogle Scholar
  30. 30.
    Rothenberg SE, Feng XB (2012) Mercury cycling in a flooded rice paddy. J Geophys Res 117, G03003Google Scholar
  31. 31.
    Downing AL, Leibold MA (2002) Ecosystem consequences of species richness and composition in pond food webs. Nature 416:837–841CrossRefPubMedGoogle Scholar
  32. 32.
    Chen D, Jing M, Wang X (2005) Determination of methyl mercury in water and soil by HPLC–ICP-MS, Agilent Technologies. 8Google Scholar
  33. 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 5:235–237PubMedCentralCrossRefPubMedGoogle Scholar
  34. 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 66:4605–4614PubMedCentralCrossRefPubMedGoogle Scholar
  35. 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 7:335–336PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  38. 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 21:494–504PubMedCentralCrossRefPubMedGoogle Scholar
  39. 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 72:5069–5072PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Connell JH (1979) Intermediate-disturbance hypothesis. Science 204:1345CrossRefPubMedGoogle Scholar
  41. 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 43–47Google Scholar
  42. 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 24:634–640CrossRefPubMedGoogle Scholar
  43. 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 30:1389–1414CrossRefGoogle Scholar
  44. 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 34:387–401CrossRefGoogle Scholar
  45. 45.
    Schultz P, Urban NR (2008) Effects of bacterial dynamics on organic matter decomposition and nutrient release from sediments: a modeling study. Ecol Model 210:1–14CrossRefGoogle Scholar
  46. 46.
    Khwaja AR, Bloom PR, Brezonik PL (2010) Binding strength of methylmercury to aquatic NOM. Environ Sci Technol 44:6151–6156CrossRefPubMedGoogle Scholar
  47. 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 64:164–173CrossRefGoogle Scholar
  48. 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 67:53–60CrossRefGoogle Scholar
  49. 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 50:58–65CrossRefGoogle Scholar
  50. 50.
    Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715CrossRefPubMedGoogle Scholar
  51. 51.
    Shrestha PM, Kube M, Reinhardt R, Liesack W (2009) Transcriptional activity of paddy soil bacterial communities. Environ Microbiol 11:960–970CrossRefPubMedGoogle Scholar
  52. 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 50:754–765CrossRefPubMedGoogle Scholar
  53. 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 30:635–644CrossRefGoogle Scholar
  54. 54.
    Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390CrossRefPubMedGoogle Scholar
  55. 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 1:453–467CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Yu-Rong Liu
    • 1
  • Jian-Jun Wang
    • 2
  • Yuan-Ming Zheng
    • 1
  • Li-Mei Zhang
    • 1
  • Ji-Zheng He
    • 1
    • 3
  1. 1.State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental SciencesChinese Academy of SciencesBeijingChina
  2. 2.State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and LimnologyChinese Academy of SciencesNanjingChina
  3. 3.Melbourne School of Land and EnvironmentUniversity of MelbourneParkvilleAustralia

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