Abstract
Bacteria are primary agents of organic substrate metabolisation and elemental cycling in landfills. Two major bacterial groups, namely, Gram-positive (GP) and Gram-negative (GN), drive independent metabolic functions that contribute to waste stabilisation. There is a lack of explicit exploration of how these different bacterial guilds respond to changing carbon (C) availability and substrate depletion as landfills age and how landfill geochemistry regulates their distribution. This study investigated and compared the abundance and vertical distribution of GP and GN bacteria in 14- and 36-year-old municipal landfills and explored linkages among bacterial groups, nutrient elements, heavy metals and soil texture. We found higher GP bacteria in the 14-year-old landfill, while GN bacteria dominated the 36-year-old landfill. The non-metric multidimensional scaling (nMDS) analysis showed that dissimilarities in the relative abundance of the GP and GN bacteria were linked distinctly to landfill age, and not depth. In support of this inference, we further found that GP and GN bacteria were negatively correlated with heavy metals and essential nutrients in the 14- and 36-year-old landfills, respectively. Notably, the GP/GN ratio, an indicator of relative C available for bacterial mineralisation, was greater in the14-year-old landfill, suggesting greater C availability. Conversely, the C to N ratio was higher in the 36-year-old landfill, indicating lower N mineralisation. Collectively, the results of the study reveal key insights into how landfill ageing and stabilisation influence distinct functional shifts in the abundance of GP and GN bacteria, and these are mainly driven by changes in C and N bioavailability.
Similar content being viewed by others
Data availability
The data obtained from the high-throughput sequencing of bacterial DNA are available in the NCBI Sequence Read Archive database (accession number PRJNA563044).
References
Abdu N, Abdullahi AA, Abdulkadir A (2017) Heavy metals and soil microbes. Environ Chem Lett 15:65–84. https://doi.org/10.1007/s10311-016-0587-x
Adelapo AO, Haris PI, Alo BI, Huddersman K, Jenkins RO (2018) Multivariate analysis of the effects of age, particle size and landfill depth on heavy metal pollution content of closed and active landfill precursors. Waste Manag 78:227–37. https://doi.org/10.1016/j.wasman.2018.05.040
Andrew D, Fitak RR, Munguia-Vega A, Racolta A, Martinson VG, Dontsova K (2012) Abiotic factors shape microbial diversity in Sonoran Desert soils. Appl Environ Microbiol 78:7527–7537. https://doi.org/10.1128/AEM.01459-12
Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations (A Review). Water Air Soil Pollut 47:335–379
Barlaz MA, Schaefer MA, Ham RK (1989) Bacterial population development and chemical characteristics of refuse decomposition in a simulated sanitary landfill. Appl Environ Microbiol 55:55–65. https://doi.org/10.1128/aem.55.1.55-65.1989
Barlaz MA, Ham RK, Schaefer MA, Isaacson R (1990) Methane production from municipal refuse: a review of enhancement techniques and microbial dynamics. Crit Rev Environ Sci Technol 19(6):557–584. https://doi.org/10.1080/10643389009388384
Beeby M, Gumbart JC, Roux B, Jensen GJ (2013) Architecture and assembly of the Gram-positive cell wall. Mol Microbiol 88:664–672. https://doi.org/10.1111/mmi.12203
Bolyard SC, Reinhart DR (2016) Application of landfill treatment approaches for stabilisation of municipal waste. Waste Manag 55:22–30. https://doi.org/10.1016/j.wasman.2016.01.024
Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agron J 54:464–465. https://doi.org/10.2134/agronj1962.00021962005400050028x
Buyer JS, Teasdale JR, Roberts DP, Zasada IA, Maul JE (2010) Factors affecting soil microbial community structure in tomato cropping systems. Soil Biol Biochem 42:831e841–831e841. https://doi.org/10.1016/j.soilbio.2010.01.020
Carlyson H, Deutschbauer A, Coates J (2017) Review: Microbial metal resistance and metabolism across dynamic landscapes: high-throughput environmental microbiology. F1000Research 6(F1000 Faculty Rev):1026. https://doi.org/10.12688/f1000research.10986.1
Chen C, Khaleel SS, Huang H, Wu CH (2014) Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code Biol Med 9:1–11. https://doi.org/10.1038/nbt1486
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Eleazer WE, Odle WS, Wang YS, Barlaz MA (1997) Biodegradability of municipal solid waste components in laboratory-scale landfills. Environ Sci Technol 31:911–917. https://doi.org/10.1021/es9606788
Fanin N, Kardola P, Farrell M, Nilssona M-C, Gundalea MJ, Wardle DA (2019) The ratio of Gram-positive to Gram-negative bacterial PLFA markers as an indicator of carbon availability in organic soils. Soil Biol Biochem 128:111–114. https://doi.org/10.1016/j.soilbio.2018.10.010
Fannin CA, Roberts RD (2006) Mature landfill waste geochemical characteristics and implications for long-term secondary substance release. Geochemistry: Exploration, Environment, Analysis 6:369–377. https://doi.org/10.1144/1467-7873/06-103
Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46:834–840. https://doi.org/10.1007/BF01935534
Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643. https://doi.org/10.1099/mic.0.037143-0
Hemkemeyer M, Dohrmann AB, Christensen BT, Tebbe CC (2018) Bacterial preferences for specific soil particle size fractions revealed by community analyses. Front Microbiol 9:149. https://doi.org/10.3389/fmicb.2018.00149
Huang KC, Mukhopadhyay R, Wen B, Gitai Z, Wingreen NS (2008) Cell shape and cell-wall organization in Gram-negative bacteria. PNAS 105:19282–19287. https://doi.org/10.1073/pnas.0805309105
Janssen BH (1996) Nitrogen mineralization in relation to C:N ratio and decomposability of organic materials. Plant Soil 181:39–45. https://doi.org/10.1007/BF00011290
Jiang J, Zhang Y, Li K, Wang Q, Gong C, Li M (2013) Volatile fatty acids production from food waste: effects of pH, temperature, and organic loading rate. Bioresour Technol 143:525–530. https://doi.org/10.1016/j.biortech.2013.06.025
Kalayu G (2019) Phosphate solubilizing microorganisms: promising approach as biofertilizers. Hindawi Int J Agron 4917256:1–7. https://doi.org/10.1155/2019/4917256
Koch L (2011) Mogale City Local Municipality Final Environmental Management Framework Project Number 10310, MCLM, Krugersdorp, South Africa.
Kramer MG, Lajtha K, Aufdenkampe AK (2017) Depth trends of soil organic matter C:N and 15 N natural abundance controlled by association with minerals. Biogeochemistry 136:237–248. https://doi.org/10.1007/s10533-017-0378-x
McCauley A, Jones C, Olson-Rutz K (2017) Soil pH and organic matter. Nutr. Manage. Module 44498. Montana State University, Bozeman, MT.
Naveen BP, Mahapatra DM, Sitharam TG, Sivapullaiah PV, Ramachandra TV (2017) Physico-chemical and biological characterization of urban municipal landfill leachate. Environ Pollut 220:1–12. https://doi.org/10.1016/j.envpol.2016.09.002
Osibote A, Oputu O (2020) Fate and partitioning of heavy metals in soils from landfill sites in Cape Town, South Africa: a health risk approach to data interpretation. Environ Geochem Health. 42:283–312. https://doi.org/10.1007/s10653-019-00348-w
Östman M (2008) Ageing landfills – development and processes. (PhD Thesis) Swedish University of Agricultural Sciences, Uppsala.
Perveen N, Ayub M, Shahzad T, Siddiq MR, Memon MS, Barot S, Saeed H, Xu M (2019) Soil carbon mineralization in response to nitrogen enrichment in surface and subsurface layers in two land use types. PeerJ. 7:e7130. https://doi.org/10.7717/peerj.7130
Plaza C, Courtier-Murias D, Fernández JM, Polo A, Simpson AJ (2013) Physical, chemical, and biochemical mechanisms of soil organic matter stabilization under conservation tillage systems: a central role for microbes and microbial by-products in C sequestration. Soil Biol Biochem 57:124–134. https://doi.org/10.1016/j.soilbio.2012.07.026
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Glo FO, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219
R Core Team (2019) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
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. https://doi.org/10.1128/AEM.01541-09
Seaton FM, George PBL, Lebron I, Jones DL, Creer S, Robinson DA (2020) Soil textural heterogeneity impacts bacterial but not fungal diversity. Soil Biol Biochem 144:107766. https://doi.org/10.1016/j.soilbio.2020.107766
Sekhohola-Dlamini L, Tekere M (2020) Microbiology of municipal solid waste landfills: a review of microbial dynamics and ecological influences in waste bioprocessing. Biodegradation 31:1–21. https://doi.org/10.1007/s10532-019-09890-x
Selvarajan R, Sibanda T, Venkatachalam S, Ogola HJO, Obieze CC, Msagati TA (2019) Distribution, interaction and functional profiles of epiphytic bacterial communities from the rocky intertidal sea weeds, South Africa. Sci Rep 9:19835. https://doi.org/10.1038/s41598-019-56269-2
Shen D, Yin J, Yu X, Wang M, Long Y, Shentu J, Chen T (2017) Acidogenic fermentation characteristics of different types of protein-rich substrates in food waste to produce volatile fatty acids. Bioresour Technol 227:125–132. https://doi.org/10.1016/j.biortech.2016.12.048
Springob G, Kirchmann H (2003) Bulk soil C to N ratio as a simple measure of net N mineralization from stabilized soil organic matter in sandy arable soils. Soil Biol Biochem 35:629–632. https://doi.org/10.1016/S0038-0717(03)00052-X
Staley BF, de los Reyes FL, Barlaz MA (2012) Comparison of bacteria and archaea communities in municipal solid waste, individual refusecomponents, and leachate. FEMS Microbiol Ecol 79:465–73. https://doi.org/10.1111/j.1574-6941.2011.01239x
Tardy V, Spor A, Mathieu O, Leveque J, Terrat S, Plassart P, Regnier T, Bardgett RD, van der Putten WH, Roggero PP, Seddaiu G, Bagella S, Lemanceau P, Ranjard L, Maron P-A (2015) Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol Biochem 90:204–213. https://doi.org/10.1016/j.soilbio.2015.08.010
Trabelsi I, Horibe H, Tanaka N, Matsuto T (2000) Origin of low carbon/nitrogen ratios in leachate from old municipal solid waste landfills. Waste Manage Res., 18, 224-234. https://doi.org/10.1177/2F0734242X0001800304
Wan X, Huang Z, He Z, Yu Z, Wang M, Davis MR, Yang Y (2015) Soil C:N ratio is the major determinant of soil microbial community structure in subtropical coniferous and broadleaf forest plantations. Plant Soil 387:103–116. https://doi.org/10.1007/s11104-014-2277-4
Wenderoth DF, Reber HH (1999) Correlation between structural diversity and catabolic versatility of metal-affected prototrophic bacteria in soil. Soil Biol Biochem 31:345–352. https://doi.org/10.1016/S0038-0717(98)00132-1
Whitaker N, Ostle J, McNamara NP, Nottingham AT, Stott AW, Bardgett RD, Salinas N, Ccahuana AJQ, Meir P (2014) Microbial carbon mineralization in tropical lowland and montane forest soils of Peru. Front Microbiol 5:1–13. https://doi.org/10.3389/fmicb.2014.00720
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer
Xu S, Lu W, Liu Y, Ming Z, Liu Y, Meng R, Wang H (2017) Structure and diversity of bacterial communities in two large sanitary landfills in China as revealed by high throughput sequencing (MiSeq). Waste Manag 63:41–48. https://doi.org/10.1016/j.wasman.2016.07.047
Xue PP, Carrillo Y, Pino V, Minasny B, McBratney AB (2018) Soil properties drive microbial community structure in a large scale transect in South Eastern Australia. Sci Rep 8:11725. https://doi.org/10.1038/s41598-018-30005-8
Zainun MY, Simarani K (2018) Metagenomics profiling for assessing microbial diversity in both active and closed landfills. Sci Total Environ 616–617:269–278. https://doi.org/10.1016/j.scitotenv.2017.10.266
Zhang Q, Zhou W, Liang GQ, Sun JW, Wang XB, He P (2015) Distribution of soil nutrients, extracellular enzyme activities and microbial communities across particle-size fractions in a long-term fertilizer experiment. Appl Soil Ecol 94:9–71. https://doi.org/10.1016/j.apsoil.2015.05.00
Acknowledgements
The authors wish to acknowledge the Postdoctoral and Visiting Research fellowships awarded to Dr Lerato Sekhohola-Dlamini and Dr Henry Ogola, respectively, by the College of Agriculture and Environmental Sciences at the University of South Africa (UNISA). The authors would also like to thank the Mogale City municipal authorities for granting permission to collect samples and the Centre for High Performance Computing that provided the high computing facility for the metagenomic analysis.
Funding
The research was funded by the College of Agricultural and Environmental Sciences at the University of South Africa (UNISA).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Code availability
Not applicable.
Conflict of interest
Authors declare no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sekhohola-Dlamini, L., Dlamini, P., Selvarajan, R. et al. Influences of geochemical factors and substrate availability on Gram-positive and Gram-negative bacterial distribution and bio-processes in ageing municipal landfills. Int Microbiol 24, 311–324 (2021). https://doi.org/10.1007/s10123-021-00167-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-021-00167-z