Microbial Abundance and Activity in Biochar-Amended Landfill Cover Soils: Evidence from Large-Scale Column and Field Experiments
Publication: Journal of Environmental Engineering
Volume 143, Issue 9
Abstract
Field and laboratory studies were conducted to evaluate the impact of biochar amendment on methane oxidation rates and microbial communities in landfill cover soils. Deoxyribonucleic acid (DNA) was isolated from soil and biochar-amended soil following incubation in laboratory soil columns and from samples collected from four test plots installed within the intermediate cover of an active landfill in northeastern Illinois. Next-generation sequencing of 16SrRNA gene amplicons following polymerase chain reaction (PCR) amplification was used to assess the community composition and relative abundance of methane-oxidizing bacteria among the samples. In field soil samples from both soil and biochar-amended soil covers, Type-I methanotrophs (primarily Methylomonas and Crenothrix species) were observed and prevailed over Type-II methanotrophs in terms of relative abundance, comprising 83 to of the total methanotrophic community. Non–methane-oxidizing methylotrophs (e.g., Methylibium, Methyloversatilis, Hyphomicrobium, Bradyrhizobium) and facultative methanotrophs (e.g., Methylocella) were also detected along with obligate methanotrophs, reflecting a diverse bacterial community. Methane oxidation rates in batch assays were positively correlated with relative abundance of methanotrophs as well as methane concentration at depth in the soil at the time of sampling. These trends indicate a significant relationship between methane exposure history and methanotrophic community abundance and composition.
Get full access to this article
View all available purchase options and get full access to this article.
Acknowledgments
This research project was funded by the U.S. National Science Foundation (Grant CMMI #1200799), which is gratefully acknowledged. The authors are thankful to J. Bogner, K. Spokas, B.Y. Sadasivam, E. Schmidt, D. Mecha, D. Perzan, K. Saad, and several graduate and undergraduate research assistants for their advice and assistance during this project.
References
Amann, R. I., Ludwig, W., and Schleifer, K. H. (1995). “Phylogenetic identification and in situ detection of individual microbial cells without cultivation.” Microbiol. Rev., 59(1), 143–169.
Amaral, J. A., and Knowles, R. (1995). “Growth of methanotrophs in methane and oxygen counter gradients.” Fems Microbiol. Lett., 126(3), 215–220.
ASTM. (2010a). “Standard test method for particle-size analysis of soils.” ASTM D422, West Conshohocken, PA.
ASTM. (2010b). “Standard test methods for laboratory determination of water (moisture) content of soil and rock by mass.” ASTM D2216, West Conshohocken, PA.
ASTM. (2010c). “Standard test methods for moisture, ash, and organic matter of peat and other organic soils.” ASTM D2974, West Conshohocken, PA.
ASTM. (2010d). “Standard test methods for specific gravity of soil solids by water pycnometer.” ASTM D854, West Conshohocken, PA.
ASTM. (2013). “Standard test method for pH of soils.” ASTM D4972, West Conshohocken, PA.
Baytshtok, V., Kim, S., Yu, R., Park, H., and Chandran, K. (2008). “Molecular and biokinetic characterization of methylotrophic denitrification using nitrate and nitrite as terminal electron acceptors.” Water Sci. Technol. J. Int. Assoc. Water Pollution Res., 58(2), 359–365.
BIOM [Computer software]. Knight Lab, La Jolla, CA.
Boden, R., et al. (2011). “Complete genome sequence of the aerobic marine methanotroph Methylomonas methanica MC09.” J. Bacteriol., 193(24), 7001–7002.
Bogner, J. E., Sass, R. L., and Walter, B. P. (2000). “Model comparisons of methane oxidation across a management gradient: Wetlands, rice production systems, landfill.” Global Biogeochem. Cycles, 14(4), 1021–1033.
Bogner, J. E., Spokas, K. A., and Burton, E. A. (1999). “Temporal variations in greenhouse gas emissions at a midlatitude landfill.” J. Environ. Qual., 28(1), 278–288.
Börjesson, G., Sundh, I., and Svensson, B. (2004). “Microbial oxidation of at different temperatures in landfill cover soils.” Fems Microbiol. Ecol., 48(3), 305–312.
Bowman, J. (2006). “The methanotrophs—The families Methylococcaceae and Methylocystaceae.” The prokaryotes, Springer, New York, 266–289.
Cai, P., Huang, Q., Zhang, X., and Chen, H. (2006). “Adsorption of DNA on clay minerals and various colloidal particles from an Alfisol.” Soil Biol. Biochem., 38(3), 471–476.
Caporaso, J. G., et al. (2012). “Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms.” ISME J., 6(8), 1621–1624.
Cébron, A., et al. (2007). “Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing.” Fems Microbiol. Ecol., 62(1), 12–23.
Chen, Y., Dumont, M. G., Cébron, A., and Murrell, J. C. (2007). “Identification of active methanotrophs in a landfill cover soil through detection of expression of 16S rRNA and functional genes.” Environ. Microbiol., 9(11), 2855–2869.
Chistoserdova, L. (2011). “Methylotrophy in a lake: From metagenomics to single-organism physiology.” Appl. Environ. Microb., 77(14), 4705–4711.
Frostegard, A., et al. (1999). “Quantification of bias related to the extraction of DNA directly from soils.” Appl. Environ. Microb., 65(12), 5409–5420.
Gebert, J., Groengroeft, A., and Miehlich, G. (2003). “Kinetics of microbial landfill methane oxidation in biofilters.” Waste Manage., 23(7), 609–619.
Gebert, J., and Perner, M. (2015). “Impact of preferential methane flow through soil on microbial community composition.” Eur. J. Soil Biol., 69, 8–16.
Gebert, J., Rachor, I., Gröngröft, A., and Pfeiffer, E.-M. (2011). “Temporal variability of soil gas composition in landfill covers.” Waste Manage., 31(5), 935–945.
Gebert, J., Stralis-Pavese, N., Alawi, M., and Bodrossy, L. (2008). “Analysis of methanotrophic communities in landfill biofilters using diagnostic microarray.” Environ. Microbiol., 10(5), 1175–1188.
Graham, D. W., Chaudhary, J. A., Hanson, J. S., and Arnold, R. G. (1993). “Factors affecting competition between Type I and Type II methanotrophs in two-organism, continuous-flow reactors.” Microb. Ecol., 25(1), 1–17.
Hanson, R. S., and Hanson, T. E. (1996). “Methanotrophic bacteria.” Microbiol. Rev., 60(2) 439–471.
Henckel, T., Roslev, P., and Conrad, R. (2000). “Effects of and on presence and activity of the indigenous methanotrophic community in rice field soil.” Environ. Microbiol., 2(6), 666–679.
Henneberger, R., Chiri, E., Bodelier, P. E. L., Frenzel, P., Lüke, C., and Schroth, M. H. (2015). “Field-scale tracking of active methane-oxidizing communities in a landfill cover soil reveals spatial and seasonal variability.” Environ. Microbiol., 17(5), 1721–1737.
Hernandez, M. E., Beck, D. A., Lidstrom, M. E., and Chistoserdova, L. (2015). “Oxygen availability is a major factor in determining the composition of microbial communities involved in methane oxidation.” Peer J., 3, e801.
Holm, N. C., Gliesche, C. G., and Hirsch, P. (1996). “Diversity and structure of hyphomicrobium populations in a sewage treatment plant and its adjacent receiving lake.” Appl. Environ. Microb., 62(2), 522–528.
Huber-Humer, M., Gebert, J., and Hilger, H. (2008). “Biotic systems to mitigate landfill methane emissions.” Waste Manage. Res., 26(1), 33–46.
Jin, H. (2010). “Characterization of microbial life colonizing biochar and biochar-amended soils.” Ph.D. dissertation, Cornell Univ., Ithaca, NY.
Kallistova, A. Y., et al. (2007). “Enumeration of methanotrophic bacteria in the cover soil of an aged municipal landfill.” Microb. Ecol., 54(4), 637–645.
Knief, C. (2015). “Diversity and habitat preferences of cultivated and uncultivated aerobic methanotrophic bacteria evaluated based on pmoA as molecular marker.” Front. Microbiol., 6, 1346.
Kolb, S. (2009). “The quest for atmospheric methane oxidizers in forest soils.” Environ. Microbiol. Rep., 1(5), 336–346.
Kolb, S., Knief, C., Dunfield, P. F., and Conrad, R. (2005). “Abundance and activity of uncultured methanotrophic bacteria involved in the consumption of atmospheric methane in two forest soils.” Environ. Microbiol., 7(8), 1150–1161.
Kumaresan, D., Abell, G. C. J., Bodrossy, L., Stralis-Pavese, N., and Murrell, J. C. (2009). “Spatial and temporal diversity of methanotrophs in a landfill cover soil are differentially related to soil abiotic factors.” Environ. Microbiol. Rep., 1(5), 398–407.
Leite, D. C. A., et al. (2014). “Comparison of DNA extraction protocols for microbial communities from soil treated with biochar.” Braz. J. Microbiol., 45(1), 175–183.
Le Mer, J., and Roger, P. (2001). “Production, oxidation, emission and consumption of methane by soils: A review.” Eur. J. Soil Biol., 37(1), 25–50.
Li, H., Chi, Z. F., Lu, W. J., and Wang, H. T. (2013). “Mitigating emissions in semi-aerobic landfills: Impacts of operating conditions on abundance and community structure of methanotrophs in cover soils.” J. Microbiol. Biotechnol., 23(7), 993–1003.
Long, X.-E., Wang, J., Huang, Y., and Yao, H. (2016). “Microbial community structures and metabolic profiles response differently to physiochemical properties between three landfill cover soils.” Environ. Sci. Pollut. Res., 23(15), 15483–15494.
Murrell, J. C. (2010). “The aerobic methane oxidizing bacteria (methanotrophs).” Handbook of hydrocarbon and lipid microbiology, K. N. Timmis, ed., Springer, Berlin, 1953–1966.
Noyce, G. L., Winsborough, C., Fulthorpe, R., and Basiliko, N. (2016). “The microbiomes and metagenomes of forest biochars.” Sci. Rep., 6(1), 26425.
OriginPro [Computer software]. OriginLab Corporation, Northampton, MA.
PEAR [Computer software]. GitHub, Inc., San Francisco.
Pietramellara, G., Franchi, M., Gallori, E., and Nannipieri, P. (2001). “Effect of molecular characteristics of DNA on its adsorption and binding on homoionic montmorillonite and kaolinite.” Biol. Fert. Soils., 33(5), 402–409.
QIIME [Computer software]. Knight Lab, La Jolla, CA.
Reddy, K. R., Yargicoglu, E. N., Yue, D., and Yaghoubi, P. (2017). “Enhanced microbial methane oxidation in landfill cover soil amended with biochar.” J. Geotech. Geoenviron. Eng.,04014047.
Röwer, I. U., Geck, C., Gebert, J., and Pfeiffer, E.-M. (2011). “Spatial variability of soil gas concentration and methane oxidation capacity in landfill covers.” Waste Manage., 31(5), 926–934.
Sadasivam, B. Y., and Reddy, K. R. (2014). “Landfill methane oxidation in soil and bio-based cover systems: A review.” Rev. Environ. Sci. Biotechnol., 13(1), 79–107.
Scheutz, C., et al. (2009). “Microbial methane oxidation processes and technologies for mitigation of landfill gas emissions.” Waste Manage. Res., 27(5), 409–455.
Scheutz, C., Mosbæk, H., and Kjeldsen, P. (2004). “Attenuation of methane and volatile organic compounds in landfill soil covers.” J. Environ. Qual., 33(1), 61–71.
Semrau, J. D. (2011). “Current knowledge of microbial community structures in landfills and its cover soils.” Appl. Microbiol. Biotechnol., 89(4), 961–969.
Semrau, J. D., Dispirito, A. A., and Yoon, S. (2010). “Methanotrophs and copper.” Fems Microbiol. Rev., 34(4), 496–531.
Stralis-Pavese, N., et al. (2004). “Optimization of diagnostic microarray for application in analysing landfill methanotroph communities under different plant covers.” Environ. Microbiol., 6(4), 347–363.
Su, Y., et al. (2014). “Diversity and activity of methanotrophs in landfill cover soils with and without landfill gas recovery systems.” Syst. Appl. Microbiol., 37(3), 200–207.
Suzuki, M. T., and Giovannoni, S. J. (1996). “Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR.” Appl. Environ. Microb., 62(2), 625–630.
Takada-Hoshino, Y., and Matsumoto, N. (2004). “An improved DNA extraction method using skim milk from soils that strongly adsorb DNA.” Microbes. Environ., 19(1), 13–19.
Theis, J., and Suzuki, K. (2003). Amazonian dark earths biological measurements, Springer, Dordrecht, Netherlands, 287–332.
Trotsenko, Y. A., and Murrell, J. C. (2008). Metabolic aspects of aerobic obligate methanotrophy, Elsevier Science and Technology, San Diego, 183–229.
Tsitko, I., et al. (2014). “The variation of microbial communities in a depth profile of an acidic, nutrient-poor boreal bog in southwestern Finland.” Open J. Ecol., 4(13), 28.
Wang, J., Xia, F.-F., Bai, Y., Fang, C.-R., Shen, D.-S., and He, R. (2011). “Methane oxidation in landfill waste biocover soil: Kinetics and sensitivity to ambient conditions.” Waste Manage., 31(5), 864–870.
Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). “Naïve Bayesian classifier for rapid assignment of rRNA sequences into the New Bacterial Taxonomy.” Appl. Environ. Microb., 73(16), 5261–5267.
Watzinger, A., Stemmer, M., Pfeffer, M., Rasche, F., and Reichenauer, T. G. (2008). “Methanotrophic communities in a landfill cover soil as revealed by PLFAs and respiratory quinones: Impact of high methane addition and landfill leachate irrigation.” Soil Biol. Biochem., 40(3), 751–762.
Wilshusen, J. H., Hettiaratchi, J. P. A., De Visscher, A., and Saint-Fort, R. (2004). “Methane oxidation and formation of EPS in compost: Effect of oxygen concentration.” Environ. Pollution, 129(2), 305–314.
Wise, M. G., McArthur, J. V., and Shimkets, L. J. (1999). “Methanotroph diversity in landfill soil: Isolation of novel type I and type II methanotrophs whose presence was suggested by culture-independent 16S ribosomal DNA analysis.” Appl. Environ. Microb., 65(11), 4887–4897.
Xin, J., et al. (2004). “Production of methanol from methane by methanotrophic bacteria.” Biocatal. Biotransform., 22(3), 225–229.
Yankson, K. K., and Steck, T. R. (2009). “Strategy for extracting DNA from clay soil and detecting a specific target sequence via selective enrichment and real-time (quantitative) PCR amplification.” Appl. Environ. Microb., 75(18), 6017–6021.
Yargicoglu, E. N., and Reddy, K. R. (2015). “Review of biological diagnostic tools and their applications in geoenvironmental engineering.” Rev. Environ. Sci. Biotechnol., 14(2), 161–194.
Yargicoglu, E. N., Sadasivam, B. Y., Reddy, K. R., and Spokas, K. (2015). “Physical and chemical characterization of waste wood derived biochars.” Waste Manage., 36, 256–268.
Yargicoglu, E. Y., and Reddy, K. R. (2017). “Effects of biochar and wood pellets amendments added to landfill cover soil on microbial methane oxidation: A laboratory column study.” J. Environ. Manage., 193, 19–31.
Information & Authors
Information
Published In
Journal of Environmental Engineering
Volume 143 • Issue 9 • September 2017
Copyright
©2017 American Society of Civil Engineers.
History
Received: Oct 24, 2016
Accepted: Mar 1, 2017
Published online: May 31, 2017
Published in print: Sep 1, 2017
Discussion open until: Oct 31, 2017
Authors
Metrics & Citations
Metrics
Citations
Download citation
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.