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Copper Pollution Increases the Resistance of Soil Archaeal Community to Changes in Water Regime

  • Soil Microbiology
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Abstract

Increasing efforts have been devoted to exploring the impact of environmental stresses on soil bacterial communities, but the work on the archaeal community is seldom. Here, we constructed microcosm experiments to investigate the responses of archaeal communities to the subsequent dry-rewetting (DW) disturbance in two contrasting soils (fluvo-aquic and red soil) after 6 years of copper pollution. Ten DW cycles were exerted on the two soils with different copper levels, followed by a 6-week recovery period. In both soils, archaeal diversity (Shannon index) in the high copper-level treatments increased over the incubation period, and archaeal community structure changed remarkably as revealed by the non-metric multidimensional scaling ordinations. In both soils, copper pollution altered the response of dominant operational taxonomic units (OTUs) to the DW disturbance. Throughout the incubation and recovery period, the resistance of archaeal abundance to the DW disturbance was higher in the copper-polluted soils than soils without pollution. Taken together, copper pollution altered the response of soil archaeal diversity and community composition to the DW disturbance and increased the resistance of the archaeal abundance. These findings have important implications for understanding soil microbial responses to ongoing environmental change.

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References

  1. Yao SH, Zhang B, Hu F (2011) Soil biophysical controls over rice straw decomposition and sequestration in soil: the effects of drying intensity and frequency of drying and wetting cycles. Soil Biol. Biochem. 43:590–599

    Article  CAS  Google Scholar 

  2. Hu HW, Chen D, He JZ (2015) Microbial regulation of terrestrial nitrous oxide formation: understanding the biological pathways for prediction of emission rates. FEMS Microbiol. Rev. 39:729–749

    Article  CAS  PubMed  Google Scholar 

  3. Hu HW, Macdonald CA, Trivedi P, Holmes B, Bodrossy L, He JZ, Singh BK (2015) Water addition regulates the metabolic activity of ammonia oxidizers responding to environmental perturbations in dry subhumid ecosystems. Environ. Microbiol. 17:444–461

    Article  CAS  PubMed  Google Scholar 

  4. Li J, Wang JT, Hu HW, Ma YB, Zhang LM, He JZ (2016) Copper pollution decreases the resistance of soil microbial community to subsequent dry–rewetting disturbance. J. Environ. Sci. 39:155–164

    Article  Google Scholar 

  5. Ma K, Conrad R, Lu Y (2012) Responses of methanogen mcrA genes and their transcripts to an alternate dry/wet cycle of paddy field soil. Appl. Environ. Microbiol. 78:445–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Philippot L, Cregut M, Chèneby D, Bressan M, Dequiet S, Martin-Laurent F, Ranjard L, Lemanceau P (2008) Effect of primary mild stresses on resilience and resistance of the nitrate reducer community to a subsequent severe stress. FEMS Microbiol. Lett. 285:51–57

    Article  CAS  PubMed  Google Scholar 

  7. Tobor-Kapłon MA, Bloem J, Römkens PF, de Ruiter PC (2006) Functional stability of microbial communities in contaminated soils near a zinc smelter (Budel, The Netherlands). Ecotoxicology 15:187–197

    Article  PubMed  Google Scholar 

  8. Mertens J, Springael D, deTroyer I, Cheyns K, Wattiau P, Smolders E (2006) Long-term exposure to elevated zinc concentrations induced structural changes and zinc tolerance of the nitrifying community in soil. Environ. Microbiol. 8:2170–2178

    Article  CAS  PubMed  Google Scholar 

  9. Griffiths BS, Philippot L (2012) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 37:112–129

    Article  PubMed  Google Scholar 

  10. Li J, Zheng YM, Liu YR, Ma YB, Hu HW, He JZ (2014) Initial copper stress strengthens the resistance of soil microorganisms to a subsequent copper stress. Microb. Ecol. 67:931–941

    Article  CAS  PubMed  Google Scholar 

  11. Fierer N, Schimel JP (2002) Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol. Biochem. 34:777–787

    Article  CAS  Google Scholar 

  12. Cao P, Zhang LM, Shen JP, Zheng YM, Di HJ, He JZ (2012) Distribution and diversity of archaeal communities in selected Chinese soils. FEMS Microbiol. Ecol. 80:146–158

    Article  CAS  PubMed  Google Scholar 

  13. He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di HJ (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol. 9:2364–2374

    Article  CAS  PubMed  Google Scholar 

  14. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol G, Prosser J, Schuster S, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  CAS  PubMed  Google Scholar 

  15. He JZ, Hu HW, Zhang LM (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol. Biochem. 55:146–154

    Article  CAS  Google Scholar 

  16. Hu HW, Xu ZH, He JZ (2014) Ammonia-oxidizing archaea play a predominant role in acid soil nitrification. Adv. Agron. 125:261–302

    Article  Google Scholar 

  17. Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 6:1032–1045

    Article  CAS  PubMed  Google Scholar 

  18. Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591

    Article  CAS  PubMed  Google Scholar 

  19. Zhou ZY, Fan YP, Wang MJ (2000) Heavy metal contamination in vegetables and their control in China. Food Rev Int 16:239–255

    Article  CAS  Google Scholar 

  20. Ma Y, Lombi E, Oliver IW, Nolan AL, McLaughlin MJ (2006) Long-term aging of copper added to soils. Environ Sci Technol 40:6310–6317

    Article  CAS  PubMed  Google Scholar 

  21. Degens BP, Schipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol. Biochem. 33:1143–1153

    Article  CAS  Google Scholar 

  22. Herfort L, Schouten S, Abbas B, Veldhuis MJ, Coolen MJ, Wuchter C, Boon JP, Herndl GJ, Damsté JSS (2007) Variations in spatial and temporal distribution of archaea in the North Sea in relation to environmental variables. FEMS Microbiol. Ecol. 62:242–257

    Article  CAS  PubMed  Google Scholar 

  23. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  25. Field D, Tiwari B, Booth T, Houten S, Swan D, Bertrand N, Thurston M (2006) Open software for biologists: from famine to feast. Nat. Biotechnol. 24:801–804

    Article  CAS  PubMed  Google Scholar 

  26. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72:5069–5072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267

    Article  CAS  PubMed  Google Scholar 

  28. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261–5267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Orwin KH, Wardle DA (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol. Biochem. 36:1907–1912

    Article  CAS  Google Scholar 

  30. Hooper DU, Chapin III FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75:3–35

    Article  Google Scholar 

  31. Yang H, Jiang L, Li LH, Li A, Wu MY, Wan SQ (2012) Diversity-dependent stability under mowing and nutrient addition: evidence from a 7-year grassland experiment. Ecol. Lett. 15:619–626

    Article  PubMed  Google Scholar 

  32. Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity-function relationships. Eur. J. Soil Sci. 62:105–116

    Article  CAS  Google Scholar 

  33. Chan H, Babayan V, Blyumin E, Gandhi C, Hak K, Harake D, Kumar K, Lee P, Li TT, Liu HY (2010) The p-type ATPase superfamily. J. Mol. Microbiol. Biotechnol. 19:5–104

    Article  CAS  PubMed  Google Scholar 

  34. Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S, Rychlik N, Nowka B, Schmeisser C, Lebedeva EV, Rattei T (2012) The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14:3122–3145

    Article  CAS  PubMed  Google Scholar 

  35. Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. The ISME J 6:847–862

    Article  CAS  PubMed  Google Scholar 

  36. Griffiths BS, Philippot L (2013) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol. Rev. 37:112–129

    Article  CAS  PubMed  Google Scholar 

  37. Rusk JA, Hamon RE, Stevens DP, McLaughlin MJ (2004) Adaptation of soil biological nitrification to heavy metals. Environ Sci Technol 38:3092–3097

    Article  CAS  PubMed  Google Scholar 

  38. Ruyters S, Mertens J, Springael D, Smolders E (2010) Stimulated activity of the soil nitrifying community accelerates community adaptation to Zn stress. Soil Biol. Biochem. 42:766–772

    Article  CAS  Google Scholar 

  39. Besaury L, Ghiglione JF, Quillet L (2014) Abundance, activity, and diversity of archaeal and bacterial communities in both uncontaminated and highly copper-contaminated marine sediments. Mar. Biotechnol. 16:230–242

    Article  CAS  PubMed  Google Scholar 

  40. Bai R, Xi D, He JZ, Hu HW, Fang YT, Zhang LM (2015) Activity, abundance and community structure of anammox bacteria along depth profile s in three different paddy soils. Soil Biol. Biochem. 91:212–221

    Article  CAS  Google Scholar 

  41. Vasileiadis S, Coppolecchia D, Puglisi E, Balloi A, Mapelli F, Hamon RE, Daffonchio D, Trevisan M (2012) Response of ammonia oxidizing bacteria and archaea to acute zinc stress and different moisture regimes in soil. Microb. Ecol. 64:1028–1037

    Article  CAS  PubMed  Google Scholar 

  42. Martin DD, Ciulla RA, Roberts MF (1999) Osmoadaptation in archaea. Appl. Environ. Microbiol. 65:1815–1825

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Fundamental Research Funds for the Central Non-profit Research Institution of CAF (CAFYBB2016QA020)and the Strategic Priority Research Program Chinese Academy of Sciences (XDB15020200).

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Correspondence to Yu-Rong Liu.

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Li, J., Liu, YR., Cui, LJ. et al. Copper Pollution Increases the Resistance of Soil Archaeal Community to Changes in Water Regime. Microb Ecol 74, 877–887 (2017). https://doi.org/10.1007/s00248-017-0992-0

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  • DOI: https://doi.org/10.1007/s00248-017-0992-0

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