Sanitary landfill improved CNPS microbial functional gene abundance compared to non-sanitary landfill

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The landfill soil microbes related to nutrient cycling, such as carbon (C), nitrogen (N), phosphorus (P), and sulfur (S) cycling, are changed by continuous waste decomposition. Monitoring the changes that occur in CNPS functional genes in different types of landfill cover soils as a whole is vital to our understanding of microbial function in element cycling.

Materials and methods

The high-throughput quantitative polymerase chain reaction–based chip (HT-Q-PCR) method was used to explore differences in the abundance of 71 CNPS functional genes in cover soils (0–20 cm, 20–40 cm, and 40–60 cm) from two types of landfills (sanitary and non-sanitary) and to examine the soil pH and the concentrations of C, N, P, S, and 6 heavy metals.

Results and discussion

The absolute abundances of CNPS functional genes varied greatly, with the highest gene abundance reaching 5.28 × 109 copies per gram of soil, and 11% (8/71) of the genes not detected. Among the detected genes, there was a much higher functional gene abundance in the sanitary landfill than in the non-sanitary landfill cover soils, and the difference in gene abundance became more significant with increasing sampling depth. In addition to landfill type and sampling depth, the soil pH, soil dissolved organic carbon (DOC), available N (AN), and available S (AS) correlated significantly to functional gene abundance. Conversely, soil heavy metals, such as Cu, Cd, Cr, Zn, and Ni, had no effects on functional gene abundance, which might be due to their low contents.


Our results suggest that sanitary landfill increases soil CNPS gene abundance compared to that of non-sanitary landfill. The findings provide suggestions for landfill treatment and ecological protection, especially regarding vegetation restoration.

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  1. Bao SD (1999) Analytical methods of soil agrochemistry (in Chinese). China Agricultural Press, Beijing, pp 30–83

  2. Bareither CA, Wolfe GL, McMahon KD, Benson CH (2013) Microbial diversity and dynamics during methane production from municipal solid waste. Waste Manag 33:1982–1992

  3. Beattie RE, Henke W, Campa MF, Hazen TC, McAliley LR, Campbell JH (2018) Variation in microbial community structure correlates with heavy-metal contamination in soils decades after mining ceased. Soil Biol Biochem 126:57–63

  4. Bhattacharyya P, Mitra A, Chakrabarti K, Chattopadhyay DJ, Chakraborty A, Kim KJEM (2008) Effect of heavy metals on microbial biomass and activities in century old landfill soil. Environ Monit Assess 136:299–306

  5. Bhattarai A, Bhattarai B, Pandey S (2015) Variation of soil microbial population in different soil horizons. J Microbiol Exp 2:00044

  6. Chang CY, Tung HH, Tseng IC, Wu JH, Liu YF, Lin HM (2010) Dynamics of methanotrophic communities in tropical alkaline landfill upland soil. Appl Soil Ecol 46:192–199

  7. Chanton J, Abichou T, Langford C, Spokas K, Hater G, Green R, Goldsmith D, Barlaz MA (2011) Observations on the methane oxidation capacity of landfill soils. Waste Manag 31:914–925

  8. Chen XW, Wong JTF, Leung AO-W, Ng CWW, Wong MH (2017) Comparison of plant and bacterial communities between a subtropical landfill topsoil 15 years after restoration and a natural area. Waste Manag 63:49–57

  9. Chen SB, Meng W, Li SS, Zhao ZQ, Wen D (2018) Overview on current criteria for heavy metals and its hint for the revision of soil environmental quality standards in China. J Integr Agric 17:765–777

  10. Dentener F, Drevet J, Lamarque JF, Bey I, Eickhout B, Fiore AM, Hauglustaine D, Horowitz LW, Krol M, Kulshrestha U (2006) Nitrogen and sulfur deposition on regional and global scales: a multimodel evaluation. Glob Biogeochem Cycles 20:GB4003/1–GB4003/21

  11. Du Y, Feng H, Zhang K, Hu LF, Fang CR, Shen DS, Long YY (2014) Role of iron in H2S emission behavior during the decomposition of biodegradable substrates in landfill. J Hazard Mater 272:36–41

  12. Feng SJ, Gao KW, Chen YX, Li Y, Zhang L, Chen H (2017) Geotechnical properties of municipal solid waste at Laogang Landfill, China. Waste Manag 63:354–365

  13. Gebert J, Singh BK, Pan Y, Bodrossy L (2009) Activity and structure of methanotrophic communities in landfill cover soils. Environ Microbiol Rep 1:414–423

  14. Harhangi HR, Mathilde LR, Theo VA, Hu BL, Joost G, Boran K, Tringe SG, Quan ZX, Jetten MS, Op den Camp HJ (2012) Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria. Appl Environ Microbiol 78:752–758

  15. Henneberger R, Lueke C, Mosberger L, Schroth MH (2012) Structure and function of methanotrophic communities in a landfill-cover soil. FEMS Microbiol Ecol 81:52–65

  16. Hu HW, Wang JT, Li J, Li JJ, Ma YB, Chen D, He JZ (2016) Field-based evidence for copper contamination induced changes of antibiotic resistance in agricultural soils. Environ Microbiol 18:3896–3909

  17. Jiao GZ, Zhang L, Zhao YC, Ma JL (2015) Optimum position of air injection in aerobic and anaerobic refuse lysimeters. Appl Mech Mater 768:318–329

  18. Jorquera M, Martinez O, Maruyama F, Marschner P, de la Luz Mora M (2008) Current and future biotechnological applications of bacterial phytases and phytase-producing bacteria. Microbes Environ 23:182–191

  19. Kaarakainen P, Meklin T, Rintala H, Hyvärinen A, Kärkkäinen P, Vepsäläinen A, Hirvonen MR, Nevalainen A (2008) Seasonal variation in airborne microbial concentrations and diversity at landfill, urban and rural sites. Clean 36:556–563

  20. Kim KD, Lee EJ (2005) Potential tree species for use in the restoration of unsanitary landfills. Environ Manag 36:1–14

  21. Kim KD, Lee EJ, Cho KH (2004) The plant community of Nanjido, a representative nonsanitary landfill in South Korea: implications for restoration alternatives. Water Air Soil Poll 154:167–185

  22. Kjeldsen P, Barlaz MA, Rooker AP, Baun A, Ledin A, Christensen TH (2002) Present and long-term composition of MSW landfill leachate: a review. Crit Rev Environ Sci Technol 32:297–336

  23. Kong JY, Su Y, Zhang QQ, Bai Y, Xia FF, Fang CR, He R (2013) Vertical profiles of community and activity of methanotrophs in landfill cover soils of different age. J Appl Microbiol 115:756–765

  24. Li YY, Chapman SJ, Nicol GW, Yao HY (2018) Nitrification and nitrifiers in acidic soils. Soil Biol Biochem 116:290–301

  25. Liao HK, Li YY, Yao HY (2018) Fertilization with inorganic and organic nutrients changes diazotroph community composition and N-fixation rates. J Soils Sediments 18:1076–1086

  26. Liu C, Cui J, Jiang G, Chen X, Wang L, Fang C (2013a) Soil heavy metal pollution assessment near the largest landfill of China. Soil Sediment Contam 22:390–403

  27. Liu L, Liu YF, Shin HD, Chen R, Li JH, Du GC, Chen J (2013b) Microbial production of glucosamine and N-acetylglucosamine: advances and perspectives. Appl Microbiol Biotechnol 97:6149–6158

  28. Long XE, Huang Y, Chi H, Li YY, Ahmad N, Yao HY (2018) Nitrous oxide flux, ammonia oxidizer and denitrifier abundance and activity across three different landfill cover soils in Ningbo, China. J Clean Prod 170:288–297

  29. Lou Z, Wang M, Zhao Y, Huang R (2015) The contribution of biowaste disposal to odor emission from landfills. J Air Waste Manage Assoc 65:479–484

  30. Lu RK (1999) Analytical methods of soil agricultural chemistry. China Agricultural Science Press, Beijing, pp 12–14 (in Chinese)

  31. Mei J, Wang L, Han D, Zhao Y (2011) Methanotrophic community structure of aged refuse and its capability for methane. J Environ Sci 23:868–874

  32. Mitsios I, Golia E, Tsadilas C (2005) Heavy metal concentrations in soils and irrigation waters in Thessaly region, Central Greece. Commun Soil Sci Plan 36:487–501

  33. Ratliff TJ, Fisk MC (2016) Phosphatase activity is related to N availability but not P availability across hardwood forests in the northeastern United States. Soil Biol Biochem 94:61–69

  34. Scheutz C, Mosbaek H, Kjeldsen P (2004) Attenuation of methane and volatile organic compounds in landfill soil covers. J Environ Qual 33:61–71

  35. Semrau JD (2011) Current knowledge of microbial community structures in landfills and its cover soils. Appl Microbiol Biotechnol 89:961–969

  36. Slack RJ, Gronow J, Voulvoulis N (2005) Household hazardous waste in municipal landfills: contaminants in leachate. Sci Total Environ 337:119–137

  37. Song L, Wang Y, Zhao H, Long DT (2015) Composition of bacterial and archaeal communities during landfill refuse decomposition processes. Microbiol Res 181:105–111

  38. Su JQ, Ding LJ, Xue K, Yao HY, Quensen J, Bai SJ, Wei WX, Wu JS, Zhou J, Tiedje JM (2015) Long-term balanced fertilization increases the soil microbial functional diversity in a phosphorus-limited paddy soil. Mol Ecol 24:136–150

  39. Tao Z, Bian R, Chai X (2018) Methylmercury levels in cover soils from two landfills in Xi’an and Shanghai, China: implications for mercury methylation potentials. Waste Manag 78:331–336

  40. Taylor SC, Mrkusich EM (2014) The state of RT-quantitative PCR: firsthand observations of implementation of minimum information for the publication of quantitative real-time PCR experiments (MIQE). J Mol Microb Biotech 24:46–52

  41. Thomas DJL, Tyrrel SF, Smith R, Farrow S (2009) Bioassays for the evaluation of landfill leachate toxicity. J Toxicol Environ Health B Crit Rev 12:83–105

  42. USEPA(United States Environmental Protection Agency) (2007) EPA method 7473 (SW-846): mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrophotometry, Washington, DC

  43. Wong MH, Yu C (1989) Monitoring of Gin Drinkers’ Bay landfill, Hong Kong: II. Gas contents, soil properties, and vegetation performance on the side slope. Environ Manag 13:753–762

  44. Wong JTF, Chen XW, Mo WY, Man YB, Ng CWW, Wong MH (2016) Restoration of plant and animal communities in a sanitary landfill: a 10-year case study in Hong Kong. Land Degrad Dev 27:490–499

  45. Yao H, Bowman D, Rufty T, Shi W (2009) Interactions between N fertilization, grass clipping addition and pH in turf ecosystems: implications for soil enzyme activities and organic matter decomposition. Soil Biol Biochem 41:1425–1432

  46. Zainun MY, Simarani K (2018) Metagenomics profiling for assessing microbial diversity in both active and closed landfills. Sci Total Environ 616:269–278

  47. Zhang Y, Cong J, Lu H, Yang C, Yang Y, Zhou J, Li D (2014) An integrated study to analyze soil microbial community structure and metabolic potential in two forest types. PLoS One 9:e93773

  48. Zheng B, Zhu Y, Sardans J, Penuelas J, Su J (2018) QMEC: a tool for high-throughput quantitative assessment of microbial functional potential in C, N, P, and S biogeochemical cycling. Sci China Life Sci 61:1451–1462

  49. Zhu YG, Zhao Y, Li B, Huang CL, Zhang SY, Yu S, Chen YS, Zhang T, Gillings MR, Su JQ (2017) Continental-scale pollution of estuaries with antibiotic resistance genes. Nat Microbiol 2:16270

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Correspondence to Huaiying Yao or Jigang Han.

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Luo, Y., Zhang, W., Li, Y. et al. Sanitary landfill improved CNPS microbial functional gene abundance compared to non-sanitary landfill. J Soils Sediments 20, 99–108 (2020).

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  • HT-Q-PCR
  • Landfill cover soil
  • Microbial gene abundance
  • Nutrient cycling