Abstract
The anaerobic biodegradation of phenol has been realised in a sequencing batch reactor (SBR) under anaerobic conditions with phenol as sole carbon and energy source and with glucose as co-substrate. A step-change increase of phenol loading (from 100 up to 2000 mg/L of phenol concentration in the feed solution) has been applied during the acclimation phase in order to progressively induce the development of a specialised microbial consortium. This approach, combined with the dynamic sequence of operations characterising SBRs and with the high biomass retention time, led to satisfactory phenol and COD removal efficiencies with values > 70% for the highest phenol input (2000 mg/L) fed as the single carbon and energy source. Analysis of removal efficiencies and biodegradation rates suggested that the use of glucose as co-substrate did not induce a significant improvement in process performance. Kinetic tests have been performed at different initial phenol (400–1000 mg/L) and glucose (1880–0 mg/L) concentrations to kinetically characterise the developed biomass: estimated kinetic constants are suitable for application and no inhibitory effect due to high concentrations of phenol has been observed in all investigated conditions. The microbial community has been characterised at different operating conditions through molecular tools: results confirm the successful adaptation-operation approach of the microbial consortium showing a gradual increase in richness and diversity and the occurrence and selection of a high proportion of phenol-degrading genera at the end of the experimentation.
Key Points • Anaerobic phenol removal in the range of 70–99% in a sequencing batch reactor. • Negligible effect of co-substrate on removal efficiencies and biodegradation rates. • No biomass inhibition due to phenol concentration in the range of 400–1000 mg/L. • Increasing phenol loads promoted the culture enrichment of phenol-degrading genera. |
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
APHA (American Public Health Association) (2012) Standards methods for the examination of water and wastewater, 22nd edn, Washington
Arutchelvan V, Kanakasabai V, Elagovan R, Nagarajan S, Muralikrishna V (2006) Kinetics of high strength phenol degradation using Bacillus brevis. J Haz Mat B129:216–222. https://doi.org/10.1016/j.jhazmat.2005.08.040
Bakhshi Z, Najafpour G, Kariminezhad E, Pishgar R, Mousavi N, Taghizade T (2011) Growth kinetic models for phenol biodegradation in a batch culture of Pseudomonas putida. Environ Technol 32(16):1835–1841. https://doi.org/10.1080/09593330.2011.562925
Bonder MJ, Abeln S, Zaura E, Brandt BW (2012) Comparing clustering and pre-processing in taxonomy analysis. Bioinformatics 28:2891–2897. https://doi.org/10.1093/bioinformatics/bts552
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869
Capson-Tojo G, Moscoviz R, Ruiz D, Santa-Catalina G, Trably E, Rouez M, Crest M, Steyer JP, Bernet N, Delgenès JP, Escudié R (2018) Addition of granular activated carbon and trace elements to favor volatile fatty acid consumption during anaerobic digestion of food waste. Bioresour Technol 260:157–268. https://doi.org/10.1016/j.biortech.2018.03.097
Carbajo JB, Boltes K, Leton P (2010) Treatment of phenol in an anaerobic fluidized bed reactor (AFBR): continuous and batch regime. Biodegradation 21:603–613. https://doi.org/10.1007/s10532-010-9328-1
Chandana Lakshmi MVV, Sridevi V (2009) A review on biodegradation of phenol from industrial effluents. J Ind Poll Cont 25(1):13–27. http://www.icontrolpollution.com/articles/a-review-on-biodegradation-of-phenol-fromindustrial-effluents-.php?aid=37440. Accessed 27 May 2020
Chapleur O, Madigou C, Civade R, Rodolphe Y, Mazeas L, Bouchez T (2016) Increasing concentrations of phenol progressively affect anaerobic digestion of cellulose and associated microbial communities. Biodegradation 27(1):15–27. https://doi.org/10.1007/s10532-015-9751-4
Chen Y, He J, Wang YQ, Kotsopoulos TA, Kaparaju P, Zeng RJ (2016) Development of an anaerobic co-metabolic model for degradation of phenol, m-cresol and easily degradable substrate. Biochem Eng J 106:19–25. https://doi.org/10.1016/j.bej.2015.11.003
Cruz Viggi C, Simonetti S, Palma E, Pagliaccia P, Braguglia C, Fazi S, Baronti S, Navarra MA, Pettiti I, Koch C, Harnisch F, Aulenta F (2017) Enhancing methane production from food waste fermentate using biochar: the added value of electrochemical testing in pre-selecting the most effective type of biochar. Biotechnol Biofuels 10:303. https://doi.org/10.1186/s13068-017-0994-7
Daugulis AJ, Tomei MC, Guieysse B (2011) Overcoming substrate inhibition during biological treatment of mono-aromatics: recent advances in bioprocess design. Appl Microbiol Biotechnol 90:1589–1608. https://doi.org/10.1007/s00253-011-3229-z
Delgadillo-Mirquez L, Lardon L, Steyer JP, Patureau D (2011) A new dynamic model for bioavailability and cometabolism of micropollutants during anaerobic digestion. Water Res 45(15):4511–4521. https://doi.org/10.1016/j.watres.2011.05.047
Donoso-Bravo A, Rosenkranz F, Valdivia V, Ruiz-Filippi G, Chamy R (2009) Anaerobic sequencing batch reactor as an alternative for the biological treatment of wine distillery effluents. Water Sci Technol 60(5):1155–1160. https://doi.org/10.2166/wst.2009.565
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric methods for determination of sugars and related substances. Anal Biochem 28:350–356. https://doi.org/10.1021/ac60111a017
Duldhardt I, Nijenhuis I, Schauer F, Heipieper HJ (2007) Anaerobically grown Thauera aromatica, Desulfococcus multivorans, Geobacter sulfurreducens are more sensitive towards organic solvents than aerobic bacteria. Appl Microbiol Biotechnol 77:705–711. https://doi.org/10.1007/s00253-007-1179-2
Eismann F, Kuschek P, Stottmeister U (1997) Microbial phenol degradation of organic compounds in natural systems: temperature–inhibition relationships. Env Sci Pollut Res 4(4):203–207. https://doi.org/10.1007/BF02986346
Fang HHP, Chen T, Li YY, Chui HK (1996) Degradation of phenol in wastewater in an upflow anaerobic sludge blanket reactor. Water Res 30(6):1353–1360. https://doi.org/10.1016/0043-1354(95)00309-6
Fang HHP, Liang DW, Zhang T, Liu Y (2006) Anaerobic treatment of phenol in wastewater under thermophilic condition. Water Res 40:427–434. https://doi.org/10.1016/j.watres.2005.11.025
Felis GE, Dellaglio F (2007) Taxonomy of lactobacilli and bifidobacteria. Curr Issues Intest Microbiol 8(2):44–61
Firozjaee TT, Najafpour GD, Asgari A, Bakhshi Z, Pishgar R, Mousavi N (2011) Phenol biodegradation kinetics in an anaerobic batch reactor, world environmental and water resources congress 2011: bearing knowledge for sustainability, 2011, pp. 4313–4321
Franchi O, Rosenkranz F, Chamy R (2018) Key microbial populations involved in anaerobic degradation of phenol and p-cresol using different inocula. Electron J Biotechnol 3:33–38. https://doi.org/10.1016/j.ejbt.2018.08.002
Grabowski A, Tindall BJ, Bardin V, Blanchet D, Jeanthon C (2005) Petrimonas sulfuriphila gen. nov., sp. nov., a mesophilic fermentative bacterium isolated from a biodegraded oil reservoir. Int J Syst Evol Micr 55(3):1113–1121. https://doi.org/10.1099/ijs.0.63426-0
Hernandez JE, Edyvean RGJ (2008) Inhibition of biogas production and biodegradability by substituted phenolic compounds in anaerobic sludge. J Haz Mat 160:20–28. https://doi.org/10.1016/j.jhazmat.2008.02.075
Olsen I (2015) Dysgonomonas. In: Whitman WB, Rainey F, Kämpfer P, Trujillo M, Chun J, DeVos P, Hedlund B, Dedysh S (eds) Bergey’s Manual of Systematics of Archaea and Bacteria, vol 2015. Wiley, Inc, pp 1–8. https://doi.org/10.1002/9781118960608.gbm00243
Ma J, Yu L, Frear C, Zhao Q, Li X, Chen S (2013) Kinetics of psychrophilic anaerobic sequencing batch reactor treating flushed dairy manure. Bioresour Technol 131:6–12. https://doi.org/10.1016/j.biortech.2012.11.147
Madigou C, Poirier S, Bureau C, Chapleur O (2016) Acclimation strategy to increase phenol tolerance of an anaerobic microbiota. Bioresour Technol 216:77–86. https://doi.org/10.1016/j.biortech.2016.05.045
Mosca Angelucci D, Tomei MC (2015) Pentachlorophenol aerobic removal in a sequential reactor: start-up procedure and kinetic study. Environ Technol 36:327–335. https://doi.org/10.1080/09593330.2014.946099
Neufeld RD, Mack JD, Strakey JP (1980) Anaerobic phenol biokinetics. J Water Pollut Control Fed 52:2367–2377. https://www.jstor.org/stable/25040887. Accessed 27 May 2020
Pishgar R, Najafpour GD, Mousavi N, Bakhshi Z, Khorrami M (2012) Phenol biodegradation kinetics in the presence of supplimentary substrate. IJE Transc B: Applic 25(3):181–191. https://doi.org/10.5829/idosi.ije.2012.25.03b.05
Poirier S, Bize A, Bureau C, Bouchez T, Chapleur O (2016) Community shifts within anaerobic digestion microbiota facing phenol inhibition: towards early warning microbial indicators? Water Res 100:296–305. https://doi.org/10.1016/j.watres.2016.05.041
Pradeep NV, Anupama S, Navya K, Shalini HN, Idris M, Hampannavar US (2015) Biological removal of phenol from wastewaters: a mini review. Appl Water Sci 5(2):105–112. https://doi.org/10.1007/s13201-014-0176-8
Rosenkranz F, Cabrol L, Carballa M, Donoso-Bravo A, Cruz L, Ruiz-Filippi G, Chamy R, Lema JM (2013) Relationship between phenol degradation efficiency and microbial community structure in an anaerobic SBR. Water Res 47:6739–6749. https://doi.org/10.1016/j.watres.2013.09.004
Sridevi V, Chandana Lakshami MVV, Manasa M, Sravani M (2012) Metabolic pathways for the biodegradation of phenol. Int J Eng Sci Adv Technol 2(3):695–705. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.300.620&rep=rep1&type=pdf. Accessed 27 May 2020
Suidan M, Najm I, Pfeffer J, Wang Y (1988) Anaerobic biodegradation of phenol: inhibition kinetics and system stability. J Environ Eng 114(6):1359–1376. https://doi.org/10.1061/(ASCE)0733-9372(1988)114:6(1359)
Tay JH, He YX, Yan YG (2000) Anaerobic biogranulation using phenol as the sole carbon source. Water Environ Res 72:189–194. https://www.jstor.org/stable/25045357. Accessed 27 May 2020
Tomei MC, Annesini MC (2008) Biodegradation of phenolic mixtures in a sequencing batch reactor a kinetic study. Env Sci Pollut Res 15(3):188–195. https://doi.org/10.1065/espr2007.12.470
van Schie PM, Young LY (1998) Isolation and characterization of phenol-degrading denitrifying bacteria. Appl Environ Microbiol 64(7):2432–2438
van Schie PM, Young LY (2000) Biodegradation of phenol: mechanisms and applications. Bioremediat J 4(1):1–18. https://doi.org/10.1080/10588330008951128
Vaneechoutte M, Nemec A, Kämpfer P, Cools P, Wauters G (2015) Acinetobacter, Chryseobacterium, Moraxella, and other nonfermentative gram-negative rods. In: Jorgensen JH, Pfaller MA, Carroll KC, Funke G, Landry ML, Richter SS, Warnock DW (eds) Manual of clinical microbiology, 11th edn. ASM Press, Washington, pp 813–837. http://hdl.handle.net/1854/LU-5837806. Accessed 27 May 2020
Veeresh G, Kumar P, Mehrotra I (2005) Treatment of phenol and cresols in upflow anaerobic sludge blanket (UASB) process: a review. Water Res 39(1):154–170. https://doi.org/10.1016/j.watres.2004.07.028
Wang G, Wen J, Li H, Qiu C (2009) Biodegradation of phenol and m-cresol by Candida albicans PDY-07 under anaerobic condition. J Ind Microbiol Biotechnol 36:809–814. https://doi.org/10.1007/s10295-009-0555-6
Wang J, Wu B, Muñoz Sierra J, He C, Hu Z, Wang W (2020) Influence of particle size distribution on anaerobic degradation of phenol and analysis of methanogenic microbial community. Environ Sci Pollut Res 27:10391–10403. https://doi.org/10.1007/s11356-020-07665-z
Author information
Authors and Affiliations
Contributions
MCT and DMA conceived and designed the research. DMA conducted the kinetic experiments. DMA and MCT analysed the kinetic data. LB and EC designed the bacterial analysis plan. EC performed the bacterial analysis. EC and LB analysed the microbial data. DMA and EC wrote the first draft of the manuscript. MCT and LB reviewed and integrated the manuscript. All authors read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Ethical statement
This article does not contain any studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 271 kb)
Rights and permissions
About this article
Cite this article
Mosca Angelucci, D., Clagnan, E., Brusetti, L. et al. Anaerobic phenol biodegradation: kinetic study and microbial community shifts under high-concentration dynamic loading. Appl Microbiol Biotechnol 104, 6825–6838 (2020). https://doi.org/10.1007/s00253-020-10696-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10696-8