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Effects of pH and polycyclic aromatic hydrocarbon pollution on thaumarchaeotal community in agricultural soils

  • Soils, Sec 5 • Soil and Landscape Ecology • Research Article
  • Published:
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Abstract

Purpose

Thaumarchaeota is an ecologically relevant archaeal phylum which may significantly contribute to global nitrogen cycling. Thaumarchaeotal abundance, composition, and activity can be changed by soil pH and pollutants such as toxic metals. This study aims to examine the responses of thaumarchaeotal community to soil pH variation and polycyclic aromatic hydrocarbon (PAH) pollution which may co-occur in agricultural soils.

Materials and methods

Field soil samples were collected from agricultural land impacted by both acidification and PAH contamination. Thaumarchaeotal abundance and composition were assessed using molecular approaches targeting 16S rRNA or amoA genes and were linked to environmental factors by correlation and canonical correspondence analysis (CCA). To evaluate the short-term responses of Thaumarchaeota to PAHs, additional soil microcosms amended with either three selected PAHs were established. Changes in thaumarchaeotal communities during the incubation were monitored.

Results and discussion

A significant correlation between thaumarchaeotal gene abundance and soil pH was observed within field samples, with the I.1a-associated group enriched when pH <5.0. CCA suggests that the community variation was primarily related to soil pH. In contrast, the effects of PAHs were minimal. In soil microcosms, high concentrations of PAHs persisted after the 4-week incubation. Independent of the PAHs added, thaumarchaeotal amoA abundance slightly increased and the compositions were stable at the end of the incubation. This might be associated with the pollutants bioavailability and potential microbe-PAH interactions in the soil.

Conclusions

Soil pH variation strongly shapes the agricultural soil thaumarchaeotal community, whereas PAH effects appear to be marginal even in the presence of high concentrations of pollutants. The complicated interaction between soil matrix, pollutants, and Thaumarchaeota requires further study.

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References

  • Alexander M (2000) Aging, bioavailability, and overestimation of risk from environmental pollutants. Environ Sci Technol 34:4259–4265

    Article  CAS  Google Scholar 

  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008) Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    Article  CAS  Google Scholar 

  • Chang S, Hyman M, Williamson K (2002) Cooxidation of naphthalene and other polycyclic aromatic hydrocarbons by the nitrifying bacterium, Nitrosomonas europaea. Biodegradation 13:373–381

    Article  CAS  Google Scholar 

  • de Menezes A, Clipson N, Doyle E (2012) Comparative metatranscriptomics reveals widespread community responses during phenanthrene degradation in soil. Environ Microbiol 14:2577–2588

    Article  Google Scholar 

  • Großkopf R, Janssen PH, Liesack W (1998) Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosms as examined by cultivation and direct 16S rRNA gene sequence retrieval. Appl Environ Microbiol 64:960–969

    Google Scholar 

  • Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, Schloter M, Griffiths RI, Prosser JI, Nicol GW (2011) Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci 108:21206–21211

    Article  CAS  Google Scholar 

  • Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

    Article  CAS  Google Scholar 

  • Harvey RG (1991) Polycyclic aromatic hydrocarbons: chemistry and carcinogenicity. Cambridge University Press, Cambridge

    Google Scholar 

  • He J-Z, Hu H-W, Zhang L-M (2012) Current insights into the autotrophic thaumarchaeal ammonia oxidation in acidic soils. Soil Biol Biochem 55:146–154

    Article  CAS  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  CAS  Google Scholar 

  • Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeter Biodegrad 45:57–88

    Article  CAS  Google Scholar 

  • Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546

    Article  Google Scholar 

  • Lehtovirta-Morley LE, Stoecker K, Vilcinskas A, Prosser JI, Nicol GW (2011) Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci 108:15892–15897

    Article  CAS  Google Scholar 

  • Liu Y-R, Zheng Y-M, Shen J-P, Zhang L-M, He J-Z (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 

  • Lu R (2000) Analytical methods for soil and agrochemistry. China Agricultural Science and Technology Press, Beijing

    Google Scholar 

  • Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. ISME J 3:916–923

    Article  CAS  Google Scholar 

  • Mertens J, Wakelin SA, Broos K, McLaughlin MJ, Smolders E (2010) Extent of copper tolerance and consequences for functional stability of the ammonia-oxidizing community in long-term copper-contaminated soils. Environ Toxicol Chem 29:27–37

    Article  CAS  Google Scholar 

  • Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  CAS  Google Scholar 

  • Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797

    Article  CAS  Google Scholar 

  • Oton EV, Quince C, Nicol GW, Prosser JI, Gubry-Rangin C (2016) Phylogenetic congruence and ecological coherence in terrestrial Thaumarchaeota. ISME J 10:85–96

    Article  CAS  Google Scholar 

  • Pester M, Schleper C, Wagner M (2011) The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr Opin Microbiol 14:300–306

    Article  CAS  Google Scholar 

  • Pester M, Rattei T, Flechl S, Gröngröft A, Richter A, Overmann J, Reinhold-Hurek B, Loy A, Wagner M (2012) amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ Microbiol 14:525–539

    Article  CAS  Google Scholar 

  • Ping LF, Luo YM, Zhang HB, Li QB, Wu LH (2007) Distribution of polycyclic aromatic hydrocarbons in thirty typical soil profiles in the Yangtze River Delta region, east China. Environ Pollut 147:358–365

    Article  CAS  Google Scholar 

  • Prosser JI, Nicol GW (2008) Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10:2931–2941

    Article  CAS  Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

    Article  CAS  Google Scholar 

  • Rotthauwe J, Witzel K, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    CAS  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • Shen J-P, Xu Z, He J-Z (2014) Frontiers in the microbial processes of ammonia oxidation in soils and sediments. J Soils Sediments 14:1023–1029

    Article  CAS  Google Scholar 

  • Sipos AJ, Urakawa H (2016) Differential responses of nitrifying archaea and bacteria to methylene blue toxicity. Lett Appl Microbiol 62:199–206

    Article  CAS  Google Scholar 

  • Subrahmanyam G, Hu H-W, Zheng Y-M, Gattupalli A, He J-Z, Liu Y-R (2014a) Response of ammonia oxidizing microbes to the stresses of arsenic and copper in two acidic alfisols. Appl Soil Ecol 77:59–67

    Article  Google Scholar 

  • Subrahmanyam G, Shen J-P, Liu Y-R, Archana G, He J-Z (2014b) Response of ammonia-oxidizing archaea and bacteria to long-term industrial effluent-polluted soils, Gujarat, Western India. Environ Monit Assess 186:4037–4050

    Article  CAS  Google Scholar 

  • Sverdrup LE, Hagen SB, Krogh PH, van Gestel CAM (2007) Benzo(a)pyrene shows low toxicity to three species of terrestrial plants, two soil invertebrates, and soil-nitrifying bacteria. Ecotoxicol Environ Saf 66:362–368

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide. Wageningen, Biometris

    Google Scholar 

  • Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A, Urich T, Engel M, Schloter M, Wagner M, Richter A, Schleper C (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci 108:8420–8425

    Article  CAS  Google Scholar 

  • Urakawa H, Garcia JC, Barreto PD, Molina GA, Barreto JC (2012) A sensitive crude oil bioassay indicates that oil spills potentially induce a change of major nitrifying prokaryotes from the Archaea to the bacteria. Environ Pollut 164:42–45

    Article  CAS  Google Scholar 

  • Weber EB, Lehtovirta-Morley LE, Prosser JI, Gubry-Rangin C (2015) Ammonia oxidation is not required for growth of group 1.1c soil Thaumarchaeota. FEMS Microbiol Ecol. doi:10.1093/femsec/fiv001

    Google Scholar 

  • Wu Y, Conrad R (2014) Ammonia oxidation-dependent growth of group I.1b Thaumarchaeota in acidic red soil microcosms. FEMS Microbiol Ecol 89:127–134

    Article  CAS  Google Scholar 

  • Wu Y, Luo Y, Zou D, Ni J, Liu W, Teng Y, Li Z (2008) Bioremediation of polycyclic aromatic hydrocarbons contaminated soil with Monilinia sp.: degradation and microbial community analysis. Biodegradation 19:247–257

    Article  CAS  Google Scholar 

  • Wu Y, Lu L, Wang B, Lin X, Zhu J, Cai Z, Yan X, Jia Z (2011) Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil Sci Soc Am J 75:1431–1439

    Article  CAS  Google Scholar 

  • Xu SS, Liu WX, Tao S (2006) Emission of polycyclic aromatic hydrocarbons in China. Environ Sci Technol 40:702–708

    Article  CAS  Google Scholar 

  • Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl Environ Microbiol 77:4618–4625

    Article  CAS  Google Scholar 

  • Zeng J, Lin X, Zhang J, Zhu H, Chen H, Wong M (2013) Successive transformation of benzo[a]pyrene by laccase of Trametes versicolor and pyrene-degrading Mycobacterium strains. Appl Microbiol Biotechnol 97:3183–3194

    Article  CAS  Google Scholar 

  • Zhalnina K, de Quadros PD, Gano KA, Davis-Richardson A, Fagen JR, Brown CT, Giongo A, Drew JC, Sayavedra-Soto LA, Arp DJ, Camargo FAO, Daroub SH, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2013) Ca. Nitrososphaera and Bradyrhizobium are inversely correlated and related to agricultural practices in long-term field experiments. Front Microbiol 4:104

    Article  Google Scholar 

  • Zhang L-M, Hu H-W, Shen J-P, He J-Z (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  Google Scholar 

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Acknowledgments

We thank Dr. Junli Hu for his helpful suggestions to the manuscript. This study was supported by the 973 Program of Ministry of Science and Technology of China (2014CB441106), the National Natural Science Foundation of China (41371310, 41201301), and the Natural Science Foundation of Jiangsu Province (BK20131462). Y. Wu acknowledges the fellowships from the Youth Innovation Promotion Association, Chinese Academy of Sciences and the State Key Laboratory of Soil and Sustainable Agriculture (Y212000014).

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Correspondence to Xiangui Lin.

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Responsible editor: Jizheng He

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Wu, Y., Zhu, Q., Zeng, J. et al. Effects of pH and polycyclic aromatic hydrocarbon pollution on thaumarchaeotal community in agricultural soils. J Soils Sediments 16, 1960–1969 (2016). https://doi.org/10.1007/s11368-016-1390-9

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  • DOI: https://doi.org/10.1007/s11368-016-1390-9

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