Abstract
Nanomaterials (NMs) commercially used for various activities mostly end up in landfills. Reduced biogas productions reported in landfill reactors create a need for more comprehensive research on these greatly-diverse microbial pools. In order to evaluate the impact of one of the most widely-used NMs, namely nano-zinc oxide (nano-ZnO), simulated bioreactor and conventional landfills were operated using real municipal solid waste (MSW) for 300 days with addition nano-ZnO. Leachate samples were taken at different phases and analyzed by 16S rRNA gene amplicon sequencing. The bacterial communities were distinctly characterized by Cloacamonaceae (phylum WWE1), Rhodocyclaceae (phylum Proteobacteria), Porphyromonadaceae (phylum Bacteroidetes), and Synergistaceae (phylum Synergistetes). The bacterial community in the bioreactors shifted at the end of the operation and was dominated by Rhodocyclaceae. There was not a major change in the bacterial community in the conventional reactors. The methanogenic archaeal diversity highly differed between the bioreactors and conventional reactors. The dominance of Methanomicrobiaceae was observed in the bioreactors during the peak methane-production period; however, their prominence shifted to WSA2 in the nano-ZnO-added bioreactor and to Methanocorpusculaceae in the control bioreactor towards the end. Methanocorpusculaceae was the most abundant family in both conventional control and nano-ZnO-containing reactors.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdelsalam E, Samer M, Attia YA, Abdel-Hadi MA, Hassan HE, Badr Y (2016) Comparison of nanoparticles effects on biogas and methane production from anaerobic digestion of cattle dung slurry. Renew Energy 87:592–598. https://doi.org/10.1016/j.renene.2015.10.053
Austin B (2014) The family Alcaligenaceae. In: The prokaryotes. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 729–757
Avramescu ML, Rasmussen PE, Chénier M, Gardner HD (2017) Influence of pH, particle size and crystal form on dissolution behaviour of engineered nanomaterials. Environ Sci Pollut Res 24:1553–1564. https://doi.org/10.1007/s11356-016-7932-2
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. https://doi.org/10.1016/j.wasman.2012.12.013
Bolyard SC, Reinhart DR, Santra S (2013) Behavior of engineered nanoparticles in landfill leachate. Environ Sci Technol 47:8114–8122. https://doi.org/10.1021/es305175e
Bystrzejewska-Piotrowska G, Golimowski J, Urban PL (2009) Nanoparticles: their potential toxicity, waste and environmental management. Waste Manag 29:2587–2595. https://doi.org/10.1016/j.wasman.2009.04.001
Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) Correspondence QIIME allows analysis of high- throughput community sequencing data intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr 7:335–336. https://doi.org/10.1038/nmeth0510-335
Cardinali-Rezende J, Debarry RB, Colturato LFDB, Carneiro EV, Chartone-Souza E, Nascimento AMA (2009) Molecular identification and dynamics of microbial communities in reactor treating organic household waste. Appl Microbiol Biotechnol 84:777–789. https://doi.org/10.1007/s00253-009-2071-z
Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99:4044–4064. https://doi.org/10.1016/j.biortech.2007.01.057
Demirel B (2016) The impacts of engineered nanomaterials (ENMs) on anaerobic digestion processes. Process Biochem 51:308–313. https://doi.org/10.1016/j.procbio.2015.12.007
Demirel B, Scherer P (2008) The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev Environ Sci Biotechnol 7:173–190. https://doi.org/10.1007/s11157-008-9131-1
Dizaj SM, Lotfipour F, Barzegar-Jalali M, Zarrintan MH, Adibkia K (2014) Antimicrobial activity of the metals and metal oxide nanoparticles. Mater Sci Eng C 44:278–284. https://doi.org/10.1016/j.msec.2014.08.031
Eduok S, Hendry C, Ferguson R, Martin B, Villa R, Jefferson B, Coulon F (2015) Insights into the effect of mixed engineered nanoparticles on activated sludge performance. FEMS Microbiol Ecol 91:1–9. https://doi.org/10.1093/femsec/fiv082
Eduok S, Ferguson R, Jefferson B, Villa R, Coulon F (2017) Aged-engineered nanoparticles effect on sludge anaerobic digestion performance and associated microbial communities. Sci Total Environ 609:232–241. https://doi.org/10.1016/j.scitotenv.2017.07.178
Fernandes H, Viancelli A, Martins CL, Antonio RV, Costa RHR (2013) Microbial and chemical profile of a ponds system for the treatment of landfill leachate. Waste Manag 33:2123–2128. https://doi.org/10.1016/j.wasman.2012.10.024
Gryta A, Oszust K, Brzezińska M, Ziemiński K, Bilińska-Wielgus N, Frąc M (2017) Methanogenic community composition in an organic waste mixture in an anaerobic bioreactor. Int Agrophysics 31:327–338. https://doi.org/10.1515/intag-2016-0057
Han G, Shin SG, Lee J, Shin J, Hwang S (2017) A comparative study on the process efficiencies and microbial community structures of six full-scale wet and semi-dry anaerobic digesters treating food wastes. Bioresour Technol 245:869–875. https://doi.org/10.1016/j.biortech.2017.08.167
Iino T, Tamaki H, Tamazawa S, Ueno Y, Ohkuma M, Suzuki KI, Igarashi Y, Haruta S (2013) Candidatus Methanogranum caenicola: a novel methanogen from the anaerobic digested sludge, and proposal of Methanomassiliicoccaceae fam. nov. and Methanomassiliicoccales ord. nov., for a methanogenic lineage of the class Thermoplasmata. Microbes Environ 28:244–250. https://doi.org/10.1264/jsme2.ME12189
Ju F, Zhang T (2014) Novel microbial populations in ambient and mesophilic biogas-producing and phenol-degrading consortia unraveled by high-throughput sequencing. Microb Ecol 68:235–246. https://doi.org/10.1007/s00248-014-0405-6
Keller AA, Lazareva A (2013) Predicted releases of engineered nanomaterials: from global to regional to local. Environ Sci Technol Lett 1:65–70. https://doi.org/10.1021/ez400106t
Keller A, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15. https://doi.org/10.1007/s11051-013-1692-4
Kim SH, Kwak SY, Suzuki T (2006) Photocatalytic degradation of flexible PVC/TiO2nanohybrid as an eco-friendly alternative to the current waste landfill and dioxin-emitting incineration of post-use PVC. Polymer (Guildf) 47:3005–3016. https://doi.org/10.1016/j.polymer.2006.03.015
Kim S, Bae J, Choi O, Ju D, Lee J, Sung H, Park S, Sang BI, Um Y (2014) A pilot scale two-stage anaerobic digester treating food waste leachate (FWL): performance and microbial structure analysis using pyrosequencing. Process Biochem 49:301–308. https://doi.org/10.1016/j.procbio.2013.10.022
Lee EH, Moon KE, Kim TG, Cho KS (2014) Depth profiles of methane oxidation potentials and methanotrophic community in a lab-scale biocover. J Biotechnol 184:56–62. https://doi.org/10.1016/j.jbiotec.2014.05.006
Li J, Schiavo S, Rametta G, Miglietta ML, la Ferrara V, Wu C, Manzo S (2017) Comparative toxicity of nano ZnO and bulk ZnO towards marine algae Tetraselmis suecica and Phaeodactylum tricornutum. Environ Sci Pollut Res 24:6543–6553. https://doi.org/10.1007/s11356-016-8343-0
Long XE, Wang J, Huang Y, Yao H (2016) Microbial community structures and metabolic profiles response differently to physiochemical properties between three landfill cover soils. Environ Sci Pollut Res 23:15483–15494. https://doi.org/10.1007/s11356-016-6681-6
Manzo S, Rocco A, Carotenuto R, de Luca Picione F, Miglietta ML, Rametta G, di Francia G (2011) Investigation of ZnO nanoparticles’ ecotoxicological effects towards different soil organisms. Environ Sci Pollut Res 18:756–763. https://doi.org/10.1007/s11356-010-0421-0
Mu H, Chen Y (2011) Long-term effect of ZnO nanoparticles on waste activated sludge anaerobic digestion. Water Res 45:5612–5620. https://doi.org/10.1016/j.watres.2011.08.022
Mueller NC, Nowack B (2008) Exposure modelling of engineered nanoparticles in the environment. Environ Sci Technol 42:44447–44453. https://doi.org/10.1021/es7029637
Myer PR, Wells JE, Smith TPL, Kuehn LA, Freetly HC (2015) Microbial community profiles of the colon from steers differing in feed efficiency. Springerplus 4:454. https://doi.org/10.1186/s40064-015-1201-6
Nobu MK, Narihiro T, Kuroda K, Mei R, Liu WT (2016) Chasing the elusive Euryarchaeota class WSA2: genomes reveal a uniquely fastidious methyl-reducing methanogen. ISME J 10:2478–2487. https://doi.org/10.1038/ismej.2016.33
Oren A (2014) The family Rhodocyclaceae. In: The prokaryotes. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 975–998
Oren A (2014b) The family Methanomicrobiaceae. In: Rosenberg E, DeLong EF, Lory S et al (eds) The prokaryotes: other major lineages of bacteria and the archaea. Springer, Berlin, Heidelberg, pp 231–246
Oren A (2014c) The family Methanocorpusculaceae. In: Rosenberg E, DeLong EF, Lory S et al (eds) The prokaryotes: other major lineages of bacteria and the archaea. Springer, Berlin, Heidelberg, pp 225–230
Otero-González L, Field JA, Sierra-Alvarez R (2014) Fate and long-term inhibitory impact of ZnO nanoparticles during high-rate anaerobic wastewater treatment. J Environ Manag 135:110–117. https://doi.org/10.1016/j.jenvman.2014.01.025
Ozbayram EG, Kleinsteuber S, Nikolausz M, Ince B, Ince O (2017) Effect of bioaugmentation by cellulolytic bacteria enriched from sheep rumen on methane production from wheat straw. Anaerobe 46:122–130. https://doi.org/10.1016/j.anaerobe.2017.03.013
Padmavathy N, Vijayaraghavan R (2008) Enhanced bioactivity of ZnO nanoparticles - an antimicrobial study. Sci Technol Adv Mater 9:035004. https://doi.org/10.1088/1468-6996/9/3/035004
Palleroni NJ (1981) Introduction to the family Pseudomonadaceae. In: Starr MP, Stolp H, Trüper HG et al (eds) The prokaryotes: a handbook on habitats, isolation, and identification of Bacteria. Springer, Berlin, Heidelberg, pp 655–665
Pohland FG, Kim JC (1999) In situ anaerobic treatment of leachate in landfill bioreactors. Water Sci Technol 40:203 LP–203210
Rekha K, Nirmala M, Nair MG, Anukaliani A (2010) Structural, optical, photocatalytic and antibacterial activity of zinco xide and manganese doped zinc oxide nanoparticles. Phys B Condens Matter 405:3180–3185. https://doi.org/10.1016/j.physb.2010.04.042
Sakarya K, Akyol Ç, Demirel B (2015) The effect of short-term exposure of engineered nanoparticles on methane production during mesophilic anaerobic digestion of primary sludge. Water Air Soil Pollut 226:100. https://doi.org/10.1007/s11270-015-2366-x
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
Song R, Shi Q, Abdrabboh GAA, Wei R (2017) Characterization and antibacterial activity of the nanocomposite of half-fin anchovy (Setipinna taty) hydrolysates/zinc oxide nanoparticles. Process Biochem 62:223–230. https://doi.org/10.1016/j.procbio.2017.07.002
Stamps BW, Lyles CN, Suflita JM, Masoner JR, Cozzarelli IM, Kolpin DW, Stevenson BS (2016) Municipal solid waste landfills harbor distinct microbiomes. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00534
Temizel İ, Emadian SM, Di Addario M et al (2017) Effect of nano-ZnO on biogas generation from simulated landfills. Waste Manag 63:18–26. https://doi.org/10.1016/j.wasman.2017.01.017
Wang X, Cao A, Zhao G, Zhou C, Xu R (2017) Microbial community structure and diversity in a municipal solid waste landfill. Waste Manag 66:79–87. https://doi.org/10.1016/j.wasman.2017.04.023
Wilkins D, Rao S, Lu X, Lee PKH (2015) Effects of sludge inoculum and organic feedstock on active microbial communities and methane yield during anaerobic digestion. Front Microbiol 6. https://doi.org/10.3389/fmicb.2015.01114
Xie Y, He Y, Irwin PL, Jin T, Shi X (2011) Antibacterial activity and mechanism of action of zinc oxide nanoparticles against campylobacter jejuni. Appl Environ Microbiol 77:2325–2331. https://doi.org/10.1128/AEM.02149-10
Xie B, Xiong S, Liang S, Hu C, Zhang X, Lu J (2012) Performance and bacterial compositions of aged refuse reactors treating mature landfill leachate. Bioresour Technol 103:71–77. https://doi.org/10.1016/j.biortech.2011.09.114
Yang Y, Xu M, Wall JD, Hu Z (2012) Nanosilver impact on methanogenesis and biogas production from municipal solid waste. Waste Manag 32:816–825. https://doi.org/10.1016/j.wasman.2012.01.009
Yang Y, Gajaraj S, Wall JD, Hu Z (2013a) A comparison of nanosilver and silver ion effects on bioreactor landfill operations and methanogenic population dynamics. Water Res 47:3422–3430. https://doi.org/10.1016/j.watres.2013.03.040
Yang Y, Zhang C, Hu Z (2013b) Impact of metallic and metal oxide nanoparticles on wastewater treatment and anaerobic digestion. Environ Sci Process Impacts 15:39–48. https://doi.org/10.1039/c2em30655g
Yazici Guvenc S, Alan B, Adar E, Bilgili MS (2017) The impact of nanoparticles on aerobic degradation of municipal solid waste. Waste Manag Res 35:426–436. https://doi.org/10.1177/0734242X17695884
Acknowledgments
We thank İlknur Temizel for sample collection and preservation.
Funding
This work was funded by Boğaziçi University Research Fund Project (project no. 13081) and TUBITAK (project no. 112Y322).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Robert Duran
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 429 kb)
Rights and permissions
About this article
Cite this article
Akyol, Ç., Ozbayram, E.G., Demirel, B. et al. Linking nano-ZnO contamination to microbial community profiling in sanitary landfill simulations. Environ Sci Pollut Res 26, 13580–13591 (2019). https://doi.org/10.1007/s11356-019-04906-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-04906-8