an official journal of: published by:
Editor in Chief: RAFFAELLO COSSU

CHARACTERISATION OF BACTERIAL DIVERSITY IN FRESH AND AGED SEWAGE SLUDGE BIOSOLIDS USING NEXT GENERATION SEQUENCING

  • Karen Ruth Little - Chemistry, Monash University, Australia
  • Han Ming Gan - Faculty of Science and Technology, Deakin University, Australia
  • Aravind Surapaneni - South East Water Ltd, Australia
  • Jonathan Schmidt - South East Water Ltd, Australia
  • Antonio Frank Patti - School of Chemistry, Monash University, Australia

DOI 10.31025/2611-4135/2020.13914

Released under CC BY-NC-ND

Copyright: © 2019 CISA Publisher

Editorial History

  • Received: 11 Aug 2019
  • Revised: 23 Jan 2020
  • Accepted: 27 Jan 2020
  • Available online: 05 Mar 2020

Abstract

Sewage sludge, often referred to as biosolids, is generated in large quantities by wastewater treatment plants. It contains macro- and micronutrients which are essential for plant growth and so represents a valuable agricultural resource. Prior to land application, pathogens are carefully monitored to reduce the risk of crop and soil contamination however to date there has been limited investigation of agriculturally beneficial bacteria indigenous to the biosolids. This study investigated shifts in the composition of the bacterial community alongside the physicochemical properties of biosolids of increasing age, from freshly dewatered to those stockpiled for approximately four years. With stockpiling, there was a significant increase in ammonium content, ranging from 801 mg/kg in the fresh biosolids to 8178 mg/kg in the stockpiled biosolids and a corresponding increase in pH ranging from 6.93 to 8.21. We detected a ten-fold increase in Firmicutes, from 4% relative abundance in the fresh biosolids compared to 40% in the older, stockpiled biosolids. Plant growth promoting bacteria (PGPB) of the Proteobacteria family, particularly of the Devosia and Bradyrhizobium genera were identified in the freshly dewatered and the older, stockpiled biosolids. Land application of the biosolids studied here could reduce fertiliser costs, provide a means of pH correction to acidic soils and a potential source of bacteria beneficial for crop growth.

Keywords


References

Australian & New Zealand Biosolids Partnership. (2016). Australian & New Zealand Biosolids Partnership. Retrieved from https://www.biosolids.com.au/

Bartram, A. K., Lynch, M. D., Stearns, J. C., Moreno-Hagelsieb, G., & Neufeld, J. D. (2011). Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end Illumina reads. Applied and environmental microbiology, 77(11), 3846-3852

Bevacqua, R. F., & Mellano, V. J. (1993). Sewage sludge compost’s cumulative effects on crop growth and soil properties. Compost science & utilization, 1(3), 34-37

Bibby, K., & Peccia, J. (2013). Identification of viral pathogen diversity in sewage sludge by metagenome analysis. Environmental Science & Technology, 47(4), 1945-1951

Bibby, K., Viau, E., & Peccia, J. (2010). Pyrosequencing of the 16S rRNA gene to reveal bacterial pathogen diversity in biosolids. Water Research, 44(14), 4252-4260

Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., . . . Gordon, J. I. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335-336

Cogger, C., Forge, T., & Neilsen, G. (2006). Biosolids recycling: Nitrogen management and soil ecology. Canadian Journal of Soil Science, 86(4), 613-620

Cooper, J. L. (2005). The effect of biosolids on cereals in central New South Wales, Australia. 1. Crop growth and yield. Australian Journal of Experimental Agriculture, 45(4), 435-443.
DOI 10.1071/EA03099

Cousin, C., Grant, J., Dixon, F., Beyene, D., & van Berkum, P. (2002). Influence of biosolids compost on the bradyrhizobial genotypes recovered from cowpea and soybean nodules. Archives of Microbiology, 177(5), 427-430.
DOI 10.1007/s00203-002-0401-y

Dai, X., Yan, H., Li, N., He, J., Ding, Y., Dai, L., & Dong, B. (2016). Metabolic adaptation of microbial communities to ammonium stress in a high solid anaerobic digester with dewatered sludge. Scientific Reports, 6

Dai, Z., Liu, G., Chen, H., Chen, C., Wang, J., Ai, S., . . . Tang, C. (2019). Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. The ISME Journal, 1-14

De Vrieze, J., Gildemyn, S., Vilchez-Vargas, R., Jáuregui, R., Pieper, D. H., Verstraete, W., & Boon, N. (2015). Inoculum selection is crucial to ensure operational stability in anaerobic digestion. Applied Microbiology and Biotechnology, 99(1), 189-199

Deng, S., Wipf, H. M.-L., Pierroz, G., Raab, T. K., Khanna, R., & Coleman-Derr, D. (2019). A Plant Growth-Promoting Microbial Soil Amendment Dynamically Alters the Strawberry Root Bacterial Microbiome. Scientific Reports, 9(1), 1-15

Edgar, R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10), 996-998

Edgar, R. C., & Flyvbjerg, H. (2015). Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics, 31(21), 3476-3482

Editorial, B. (2015). Sporosarcina. In Bergey’s Manual of Systematics of Archaea and Bacteria: John Wiley & Sons, Ltd

EPA Victoria. (2004). Guidelines for Environmental Management, Biosolids Land Application

Ferraz, A. d. V., Momentel, L. T., & Poggiani, F. (2016). Soil fertility, growth and mineral nutrition in Eucalyptusgrandis plantation fertilized with different kinds of sewage sludge. New Forests, 47(6), 861-876

Ghaffari, S., Sepahi, A. A., Razavi, M. R., Malekzadeh, F., & Haydarian, H. (2011). Effectiveness of inoculation with isolated Anoxybacillus sp. MGA110 on municipal solid waste composting process. African Journal of Microbiology Research, 5(30), 5373-5378

Gómez-Muñoz, B., Magid, J., & Jensen, L. S. (2017). Nitrogen turnover, crop use efficiency and soil fertility in a long-term field experiment amended with different qualities of urban and agricultural waste. Agriculture, Ecosystems & Environment, 240, 300-313

Grady, E. N., MacDonald, J., Liu, L., Richman, A., & Yuan, Z.-C. (2016). Current knowledge and perspectives of Paenibacillus: a review. Microbial Cell Factories, 15(1), 203

Herrmann, R. F., Grosser, R. J., Farrar, D., & Brobst, R. B. (2017). Field studies measuring the aerosolization of endotoxin during the land application of Class B biosolids. Aerobiologia.
DOI 10.1007/s10453-017-9480-8

Hershey, D. M., Lu, X., Zi, J., & Peters, R. J. (2014). Functional conservation of the capacity for ent-kaurene biosynthesis and an associated operon in certain rhizobia. Journal of bacteriology, 196(1), 100-106

Hu, Y., Pang, S., Yang, J., Zhao, X., & Cao, J. (2019). Changes in soil microbial community structure following amendment of biosolids for seven years. Environmental Pollutants and Bioavailability, 31(1), 24-31.
DOI 10.1080/26395940.2019.1569478

Huang, Y., Sun, Y., Ma, S., Chen, L., Zhang, H., & Deng, Y. (2013). Isolation and characterization of Keratinibaculum paraultunense gen. nov., sp. nov., a novel thermophilic, anaerobic bacterium with keratinolytic activity. FEMS Microbiology Letters, 345(1), 56-63.
DOI 10.1111/1574-6968.12184

Irwin, R., Surapaneni, A., Smith, D., Schmidt, J., Rigby, H., & Smith, S. R. (2017). Verification of an alternative sludge treatment process for pathogen reduction at two wastewater treatment plants in Victoria, Australia. Journal of water and health, 15(4), 626-637

Janssen, P. H. (2006). Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Applied and environmental microbiology, 72(3), 1719-1728

Karpowicz, E., Novinscak, A., Bärlocher, F., & Filion, M. (2010). qPCR quantification and genetic characterization of Clostridium perfringens populations in biosolids composted for 2 years. Journal of applied microbiology, 108(2), 571-581

Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., & Glöckner, F. O. (2012). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, gks808

Lauber, C. L., Hamady, M., Knight, R., & Fierer, N. (2009). Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Applied and environmental microbiology, 75(15), 5111-5120

Li, N., Xue, Y., Chen, S., Takahashi, J., Dai, L., & Dai, X. (2017). Methanogenic population dynamics regulated by bacterial community responses to protein-rich organic wastes in a high solid anaerobic digester. Chemical Engineering Journal, 317, 444-453.
DOI 10.1016/j.cej.2017.02.098

Lowendorf, H. S., Baya, A. M., & Alexander, M. (1981). Survival of Rhizobium in acid soils. Applied and environmental microbiology, 42(6), 951-957

Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal, 17(1), pp. 10-12

McSpadden Gardener, B. B. (2004). Ecology of Bacillus and Paenibacillus spp. in Agricultural Systems. Phytopathology, 94(11), 1252-1258.
DOI 10.1094/PHYTO.2004.94.11.1252

Mörsdorf, G., & Kaltwasser, H. (1989). Ammonium assimilation in Proteus vulgaris, Bacillus pasteurii, and Sporosarcina ureae. Archives of Microbiology, 152(2), 125-131.
DOI 10.1007/bf00456089

Mossa, A.-W., Dickinson, M. J., West, H. M., Young, S. D., & Crout, N. M. J. (2017). The response of soil microbial diversity and abundance to long-term application of biosolids. Environmental Pollution, 224, 16-25.
DOI 10.1016/j.envpol.2017.02.056

Nagel, R., Bieber, J. E., Schmidt-Dannert, M. G., Nett, R. S., & Peters, R. J. (2018). A Third Class: Functional Gibberellin Biosynthetic Operon in Beta-Proteobacteria. Frontiers in Microbiology, 9(2916).
DOI 10.3389/fmicb.2018.02916

Novinscak, A., DeCoste, N., Surette, C., & Filion, M. (2009). Characterization of bacterial and fungal communities in composted biosolids over a 2 year period using denaturing gradient gel electrophoresis. Canadian journal of microbiology, 55(4), 375-387

Novinscak, A., Filion, M., Surette, C., & Allain, C. (2008). Application of molecular technologies to monitor the microbial content of biosolids and composted biosolids. Water Science and Technology, 57(4), 471-477.
DOI 10.2166/wst.2008.019

Oliveros, J. C. (2015). VENNY. An interactive tool for comparing lists with Venn Diagrams. 2007. In

Paez-Rubio, T., Ramarui, A., Sommer, J., Xin, H., Anderson, J., & Peccia, J. (2007). Emission rates and characterization of aerosols produced during the spreading of dewatered class B biosolids. Environmental Science & Technology, 41(10), 3537-3544

Petersen, S. O., Petersen, J., & Rubæk, G. H. (2003). Dynamics and plant uptake of nitrogen and phosphorus in soil amended with sewage sludge. Applied Soil Ecology, 24(2), 187-195

Qiong, L., Li, J.-m., Cui, X.-l., & Wei, D.-p. (2012). On-farm assessment of biosolids effects on nitrogen and phosphorus accumulation in soils. Journal of Integrative Agriculture, 11(9), 1545-1554

Rouch, D. A., Fleming, V., Deighton, M., Blackbeard, J., & Smith, S. R. (2008). Evaluating pathogen risks in production of biosolids in Victoria. Paper presented at the AWA Biosolids Specialty IV Conference

Sarkar, S., Banerjee, R., Chanda, S., Das, P., Ganguly, S., & Pal, S. (2010). Effectiveness of inoculation with isolated Geobacillus strains in the thermophilic stage of vegetable waste composting. Bioresource Technology, 101(8), 2892-2895

Schlatter, D. C., Paul, N. C., Shah, D. H., Schillinger, W. F., Bary, A. I., Sharratt, B., & Paulitz, T. C. (2019). Biosolids and Tillage Practices Influence Soil Bacterial Communities in Dryland Wheat. Microbial Ecology, 78(3), 737-752.
DOI 10.1007/s00248-019-01339-1

Shange, R. S., Ankumah, R. O., Ibekwe, A. M., Zabawa, R., & Dowd, S. E. (2012). Distinct Soil Bacterial Communities Revealed under a Diversely Managed Agroecosystem. PloS one, 7(7), e40338.
DOI 10.1371/journal.pone.0040338

Slattery, J., & Pearce, D. (2001). The impact of background rhizobial populations on inoculation response. Inoculates and nitrogen fixation of legumes in Vietnam. ACIAR Proceeding(109e), 37-45

Slimane, K., Fathya, S., Assia, K., & Hamza, M. (2014). Influence of Inoculums/Substrate Ratios (ISRs) on the Mesophilic Anaerobic Digestion of Slaughterhouse Waste in Batch Mode: Process Stability and Biogas Production. Energy Procedia, 50, 57-63.
DOI 10.1016/j.egypro.2014.06.007

Tamoutsidis, E., Papadopoulos, I., Tokatlidis, I., Zotis, S., & Mavropoulos, T. (2002). Wet sewage sludge application effect on soil properties and element content of leaf and root vegetables. Journal of plant nutrition, 25(9), 1941-1955

Trabelsi, D., Mengoni, A., Ben Ammar, H., & Mhamdi, R. (2011). Effect of on-field inoculation of Phaseolus vulgaris with rhizobia on soil bacterial communities. FEMS Microbiology Ecology, 77(1), 211-222.
DOI 10.1111/j.1574-6941.2011.01102.x

Viau, E., & Peccia, J. (2009a). Evaluation of the enterococci indicator in biosolids using culture-based and quantitative PCR assays. Water Research, 43(19), 4878-4887

Viau, E., & Peccia, J. (2009b). Survey of wastewater indicators and human pathogen genomes in biosolids produced by class A and class B stabilization treatments. Applied and environmental microbiology, 75(1), 164-174

Warman, P., & Termeer, W. (2005). Evaluation of sewage sludge, septic waste and sludge compost applications to corn and forage: yields and N, P and K content of crops and soils. Bioresource Technology, 96(8), 955-961

Wolińska, A., Kuźniar, A., Zielenkiewicz, U., Banach, A., Izak, D., Stępniewska, Z., & Błaszczyk, M. (2017). Metagenomic Analysis of Some Potential Nitrogen-Fixing Bacteria in Arable Soils at Different Formation Processes. Microbial Ecology, 73(1), 162-176

Yergeau, E., Masson, L., Elias, M., Xiang, S., Madey, E., Huang, H., . . . Beaudette, L. (2016). Comparison of Methods to Identify Pathogens and Associated Virulence Functional Genes in Biosolids from Two Different Wastewater Treatment Facilities in Canada. PloS one, 11(4), e0153554.
DOI 10.1371/journal.pone.0153554


nov
18
nov
16