Effect of straw on microbial community composition and degradation efficiency of polycyclic aromatic hydrocarbons in sludge digester

  • T. T. Tang
  • J. LiEmail author
  • Z. Yang
  • X. Y. Luo
  • Y. Chen
Original Paper


The main aim of this study was to investigate the effect of straw on microbial community composition and the degradation efficiency of polycyclic aromatic hydrocarbons (PAHs) in a sludge digester. In this study, three straws and four different ratios were assessed using identical semi-continuous-fed anaerobic digestion bioreactors; VSsludge/VScorn = ratio of 1:1.5 (C3) was observed to produce the highest biogas yield (2303.08 mL/d, with a methane content of 52.49 ± 2.74%). The latter yield was approximately three times greater than that of the control (536.15 mL/d, with a methane content of 37.07 ± 1.41%). However, the associated removal efficiency of PAHs was higher for other VSsludge/VScorn ratios apart from VSsludge/VSrice = 1:0.5 (R1) and VSsludge/VSwheat = 1:1.5 (W3). The highest removal rates were observed for 4-ring PAHs, especially BbF and BkF, which exhibited average removal rates of 60.87% and 67.74%, respectively. 16S rRNA gene sequencing demonstrated that Bacteroidetes, Proteobacteria and Chloroflexi were the dominant operational taxonomic units during co-digestion, and Christensenellaceae_R-7_group and unclassified_f_Ruminococcaceae increased to 2.33–15.73% and 0.61–1.74% following the addition of straw, respectively. In addition, the abundance of acetotrophic methanogens (Methanosaeta) varied with the addition of straw. Methanomassiliicoccus, which is the main methylotrophic methanogenic genus, increased in abundance from 1.00 to 8.07%.


Sludge Straw Polycyclic aromatic hydrocarbons Co-digestion 16S rRNA gene sequencing 



This work was supported by the National Natural Science Foundation of China (51508120), Guizhou Provincial Education Department (ZDXK [2016]11), Guizhou Provincial Science and Technology Department (LH [2014]7652), Young Talents of Science and Technology Incubation Project of Education Department of Guizhou Province (KY [2018]118).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abad E, Martínez K, Planas C, Palacios O, Caixach J, Rivera J (2005) Priority organic pollutant assessment of sludges for agricultural purposes. Chemosphere 61:1358–1369Google Scholar
  2. Abdel-Shafy HI, Mansour MSM (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25:107–123Google Scholar
  3. Aparicio I, Santos JL, Alonso E (2009) Limitation of the concentration of organic pollutants in sewage sludge for agricultural purposes: a case study in South Spain. Waste Manag 29:1747–1753Google Scholar
  4. APHA-AWWA-WEF (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington, DCGoogle Scholar
  5. Becker KW, Elling FJ, Yoshinaga MY, Söllinger A, Urich T, Hinrichs KU (2016) Unusual butane-and pentanetriol-based tetraether lipids in Methanomassiliicoccus luminyensis, a representative of the seventh order of methanogens. Appl Environ Microbiol 82:4505–4516Google Scholar
  6. Carrère H, Bernal-Martínez A, Patureau D, Delgenès JP (2006) Parameters explaining removal of PAHs from sewage sludge by ozonation. AIChE J 52:3612–3620Google Scholar
  7. Cersosimo LM, Bainbridge ML, Kraft J, Wright ADG (2016) Influence of periparturient and postpartum diets on rumen methanogen communities in three breeds of primiparous dairy cows. BMC Microbiol 16(1):78Google Scholar
  8. Chen S, Dong X (2005) Proteiniphilum acetatigenes gen. nov. sp. nov. from a UASB reactor treating brewery wastewater. Int J Syst Evol Microbiol 55(6):2257–2261Google Scholar
  9. Chen Y, Cheng JJ, Creamer KS (2008) Inhibition of anaerobic digestion process: a review. Bioresour Technol 99(10):4044–4064Google Scholar
  10. Clarke BO, Smith SR (2011) Review of “emerging” organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids. Environ Int 37:226–247Google Scholar
  11. Dean-Ross D, Moody J, Cerniglia CE (2002) Utilization of mixtures of polycyclic aromatic hydrocarbons by bacteria isolated from contaminated sediment. FEMS Microbiol Ecol 41(1):1–7Google Scholar
  12. Dieho K, Henderson Bogert G, Bannink A, Ramiro-Garcia J, Smidt H, Dijkstra J (2017) Changes in rumen microbiota composition and in situ degradation kinetics during the dry period and early lactation as affected by rate of increase of concentrate allowance. J Dairy Sci 100:2695–2710Google Scholar
  13. Fitamo T, Treu L, Boldrina A, Sartori C, Angelidaki I, Scheutz C (2017) Microbial population dynamics in urban organic waste anaerobic co-digestion with mixed sludge during a change in feedstock composition and different hydraulic retention times. Water Res 118:261–271Google Scholar
  14. Flint HHJ, Bayer EA, Rincon MT (2008) White Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131Google Scholar
  15. Fontes CM, Gilbert HJ (2010) Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 79:655–681Google Scholar
  16. Gerardi MH (2003) The microbiology of anaerobic digesters. Wiley, New YorkGoogle Scholar
  17. Gonzalez-Fernandez C, Sialve B, Molinuevo-Salces B (2015) Anaerobic digestion of microalgal biomass: challenges, opportunities and research needs. Bioresour Technol 198:896–906Google Scholar
  18. Hatamoto M, Kaneshige M, Nakamura A, Yamaguchi T (2014) Bacteroides luti sp. nov. an anaerobic, cellulolytic and xylanolytic bacterium isolated from methanogenic sludge. Int J Syst Evol Microbiol 64(5):1770–1774Google Scholar
  19. Henry SM, Grbic-Galic D (1991) Influence of endogenous and exogenous electron donors and trichloroethylene oxidation toxicity on trichloroethylene oxidation by methanotrophic cultures from a groundwater aquifer. Appl Environ Microbiol 57(1):236–244Google Scholar
  20. Hu JC (2003) Theory and technology of wastewater anaerobic biological treatment. China Building Industry Press, BeijingGoogle Scholar
  21. Iino T, Mori K, Suzuki K (2010) Methanospirillum lacunae sp. nov., a methane-producingarchaeon isolated from a puddly soil, and emended descriptions of the genus Methanospirillum and Methanospirillum hungatei. Int J Syst Evol Microbiol 60:2563–25666Google Scholar
  22. Imachi H, Sakai S, Ohashi A, Harada H, Hanada S, Kamagata Y, Sekiguchi Y (2007) Pelotomaculum propionicicum sp. nov., an anaerobic, mesophilic, obligately syntrophic, propionate-oxidizing bacterium. Int J Syst Evol Microbiol 57(7):1487–1492Google Scholar
  23. Ito T, Yoshiguchi K, Ariesyady HD, Okabe S (2011) Identification of a novel acetate-utilizing bacterium belonging to Synergistes group 4 in anaerobic digester sludge. ISME J 5(12):1844–1856Google Scholar
  24. Kiel M, Engesser KH (2015) The biodegradation vs. biotransformation of fluorosubstituted aromatics. Appl Microbiol Biotechnol 99:7433–7464Google Scholar
  25. Kröninger L, Berger S, Welte C, Deppenmeier U (2016) Evidence for the involvement of two heterodisulfide reductases in the energy-conserving system of Methanomassiliicoccus luminyensis. FEBS J 283:472–483Google Scholar
  26. Lee C, Kim J, Hwang K, O’Flaherty V, Hwang S (2009) Quantitative analysis of methanogenic community dynamics in three anaerobic batch digesters treating different wastewaters. Water Res 43(1):157–165Google Scholar
  27. Lemos LN, Fulthorpe RR, Triplett EW, Roesch LFW (2011) Rethinking microbial diversity analysis in the high throughput sequencing era. J Microbiol Methods 86(1):42–51Google Scholar
  28. Li K, Liu R, Sun C (2016) A review of methane production from agricultural residues in China. Renew Sustain Energy Rev 54:857–865Google Scholar
  29. Lianeza Coalla H, Blanco Fernandez JM, Moris Moran MA, López Bobo MR (2009) Biogas generation apple pulp. Bioresour Technol 100:3843–3847Google Scholar
  30. Liang L, Song X, Kong J, Shen C, Huang T, Hu Z (2014) Anaerobic biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by a facultative anaerobe Pseudomonas sp. JP1. Biodegradation 25:825–833Google Scholar
  31. Liu YL, Wang L, Ma J, Zhao XD, Huang ZS, Mahadevan GD, Qi JY (2016) Improvement of settleability and dewaterability of sludge by newly prepared alkaline ferrate solution. Chem Eng J 287:11–18Google Scholar
  32. Lu L, Xing DF, Ren NQ (2012) Pyrosequencing reveals highly diverse microbial communities in microbial electrolysis cells involved in enhanced H2 production from waste activated sludge. Water Res 46(7):2425–2434Google Scholar
  33. Luo YF, Wu YG, Wang H, Xing RR, Zheng ZL, Qiu J (2018) Bacterial community structure and diversity responses to the direct revegetation of an artisanal zinc smelting slag after 5 years. Environ Sci Pollut Res 25:14773–14788Google Scholar
  34. Mata-Alvarez J, Dosta J, Romero-Guiza MS, Fonoll X, Peces M, Astal S (2014) A critical review on anaerobic co-digestion achievements between 2010 and 2013. Renew Sustain Energy Rev 36:412–427Google Scholar
  35. Mc Nally DL, Mihelcic JR, Lueking DR (1999) Biodegradation of mixtures of polycyclic aromatic hydrocarbons under aerobic and nitrate-reducing conditions. Chemosphere 38(6):1313–1321Google Scholar
  36. Meng XZ, Venkatesan AK, Ni YL, Steele JC (2016) Organic contaminants in Chinese sewage sludge: a meta-analysis of the literature of the past 30 years. Environ Sci Technol 50(11):5454–5466Google Scholar
  37. Morotomi M, Nagai F, Watanabe Y (2011) Description of Christensenella minuta gen nov., sp. nov., isolated from human faeces, which forms a distinct branch in the order Clostridiales, and proposal of Christensenellaceae fam. nov. Int J Syst Evol Microbiol 62(1):144–149Google Scholar
  38. Morrison M, Miron J (2000) Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins? FEMS Microbiol Lett 185(2):109–115Google Scholar
  39. Mussoline W, Esposito G, Giordano A, Lens P (2013) The anaerobic digestion of rice straw: a review. Crit Rev Environ Sci Technol 43(9):895–915Google Scholar
  40. Nelson MC, Morrison M, Yu Z (2011) A meta-analysis of the microbial diversity observed in anaerobic digesters. Bioresour Technol 102(4):3730–3739Google Scholar
  41. Nielsen HB, Uellendahl H, Ahring BK (2007) Regulation and optimization of the biogas process: propionate as a key parameter. Biomass Bioenergy 31(11–12):820–830Google Scholar
  42. Petrasek AC, Kugelman IJ, Austern BM, Pressley TA, Winslow LA, Wise RH (1983) Fate of toxic organic compounds in wastewater treatment plants. J Water Pollut Control Fed 55(10):1286–1296Google Scholar
  43. Qin W, Zhu Y, Fan F, Wang YY, Liu X, Ding AZ, Dou JF (2017) Biodegradation of benzo(a)pyrene by Microbacterium sp. strain under denitrification: degradation pathway and effects of limiting electron acceptors or carbon source. Biochem Eng J 121(5):131–138Google Scholar
  44. Raposo F, Rubia MADL, Fernandez-ernandez Borja R (2012) Anaerobic digestion of solid organic substrates in batch mode: an overview relating to methane yields and experimental procedures. Renew Sustain Energy Rev 16(1):861–877Google Scholar
  45. Rivière D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J 3(6):700–714Google Scholar
  46. Robert C, Chassard C, Lawson PA, Bernalier-Donadille A (2007) Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community. Int J Syst Evol Microbiol 57(7):1516–1520Google Scholar
  47. Rowsell VF, Tangney P, Hunt C, Voulvoulis N (2009) Estimating levels of micropollutants in municipal wastewater. Water Air Soil Pollut 206:357–368Google Scholar
  48. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sabl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541Google Scholar
  49. Shah FA, Mahmood Q, Shah MM, Pervez A, Asad SA (2014) Microbial ecology of anaerobic digesters: the key players of anaerobiosis. Sci World J 2014:1–21Google Scholar
  50. Sosnowski P, Klepacz-Smolka A, Kaczorek K, Ledakowicz S (2008) Kinetic investigations of methane co-fermentation of sewage sludge and organic fraction of municipal solid wastes. Bioresour Technol 99(13):5731–5737Google Scholar
  51. Sousa DZ, Smidt H, Alves MM, Stams AJM (2007) Syntrophomonas zehnderi sp. nov., an anaerobe that degrades long-chain fatty acids in co-culture with Methanobacterium formicicum. Int J Syst Evol Microbiol 57(3):609–615Google Scholar
  52. Stams AJ, Sousa DZ, Kleerebezem R, Plugge CM (2012) Role of syntrophic microbial communities in high-rate methanogenic bioreactors. Water Sci Technol 66(2):352–362Google Scholar
  53. Sundberg C, Al-Soud WA, Larsson M, Alm E, Yekta SS, Svensson BH, Sorensen SJ, Karlsson A (2013) 454 pyrosequencing analyses of bacterial and archaeal richness in 21 full-scale biogas digesters. FEMS Microbiol Ecol 85(3):612–626Google Scholar
  54. Turker G, Aydin S, Akyol C, Yenigun O, Ince O, Ince B (2016) Changes in microbial community structures due to varying operational conditions in the anaerobic digestion of oxytetracycline-medicated cow manure. Appl Environ Microbiol 100(14):6469–6479Google Scholar
  55. Ueki A, Akasaka H, Suzuki D, Ueki K (2006) Paludibacter propionicigenes gen. nov. sp. nov. a novel strictly anaerobic, gram-negative, propionate-producing bacterium isolated from plant residue in irrigated rice-field soil in Japan. Int J Syst Evol Microbiol 56(1):39–44Google Scholar
  56. Wirth R, Kovacs E, Maroti G, Bagi Z, Rakhely G, Kovacs KL (2012) Characterization of a biogas-producing microbial community by short-read next generation DNA sequencing. Biotechnol Biofuels 5(1):41Google Scholar
  57. Yin Q, Yang S, Wang Z, Xing L, Wu G (2018) Clarifying electron transfer and metagenomic analysis of microbial community in the methane production process with the addition of ferroferric oxide. Chem Eng J 333:216–225Google Scholar
  58. Yu G, Zhang Y, Zhou X (2015) Effect of Ca(OH)2, pretreatment on extruded rice straw anaerobic digestion. Bioresour Technol 196:116–122Google Scholar
  59. Zhang QG (2005) Biogas technology and its application. Chemical Industry Press, BeijingGoogle Scholar
  60. Zheng X, Su YL, Li X, Xiao ND, Wang DB, Chen YG (2013) Pyrosequencing reveals the key microorganisms involved in sludge alkaline fermentation for efficient short-chain fatty acids production. Environ Sci Technol 47(9):4262–4268Google Scholar
  61. Zhou L, Liu X, Dong X (2014) Methanospirillum psychrodurum sp. nov., isolated from wetland soil. Int J Syst Evol Microbiol 64:638–641Google Scholar
  62. Ziganshin AM, Liebetrau J, Pröter J, Kleinsteuber S (2013) Microbial community structure and dynamics during anaerobic digestion of various agricultural waste materials. Appl Microbiol Biotechnol 97(11):5161–5174Google Scholar

Copyright information

© Islamic Azad University (IAU) 2019

Authors and Affiliations

  • T. T. Tang
    • 1
  • J. Li
    • 1
    • 2
    Email author
  • Z. Yang
    • 1
  • X. Y. Luo
    • 3
  • Y. Chen
    • 1
  1. 1.College of Resources and Environmental EngineeringGuizhou UniversityGuiyangChina
  2. 2.Karst Eco-environmental Engineering Research Center of Guizhou ProvinceGuizhou UniversityGuiyangChina
  3. 3.Guiyang Station of the National Water Quality Monitoring System for Urban Water SupplyGuiyangChina

Personalised recommendations