Biomass Profiling in a Horizontal-Flow Anaerobic Bioreactor Used for Limonene Degradation.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
24 Aug 2024
24 Aug 2024
Historique:
received:
10
06
2024
accepted:
15
08
2024
medline:
24
8
2024
pubmed:
24
8
2024
entrez:
23
8
2024
Statut:
epublish
Résumé
This study characterized the microbial community present in the bench scale horizontal-flow anaerobic immobilized biomass bioreactor (HAIB) used in the removal of limonene, a compound present in citrus processing industries. The HAIB was filled with three support materials (coal, polyurethane foam and gravel) which were inoculated with anaerobic sludge. The limonene initial concentration on the substrate ranged from 10 mg/L to 500 mg/L. The analysis of 16S rRNA showed the presence of 22 OTUs (based on ⩾97% sequence identity), distributed in 57 genera, considering three different matrices. Higher relative abundance of phyla was observed as Synergistetes (43-57%), Proteobacteria (32-42%), Firmicutes (7-8%) and Acidobacteria (2-3%). Actinobacteria, Bacterioidetes and Chloroflexi had the lowest relative abundances between 1 and 2%. Synergistaceae family was the predominated group (47.6%-mineral coal, 55.9%-foam and 43.5%-gravel) followed by Syntrophaceae (2.4%-coal, 1.5%-foam and 2.2%-gravel), which kept a syntrophic relationship with methanogenesis (hydrogenotrophic methanogens) to maintain the anaerobic digestion. Among the Proteobacteria phylum, the Pseudomonadaceae family was predominant in the system with 12.0% on coal, 13.1% on foam, and 20.4% on gravel. The metabolic versatility of Pseudomonas sp. makes them an important bioremediation agent by being capable of metabolizing xenobiotic and chemical toxic compounds, thus having great prominence for the limonene removal in the HAIB bioreactor.
Identifiants
pubmed: 39179725
doi: 10.1007/s00284-024-03849-9
pii: 10.1007/s00284-024-03849-9
doi:
Substances chimiques
Limonene
9MC3I34447
RNA, Ribosomal, 16S
0
Sewage
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
323Subventions
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2015/15880-1
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Lotito AM, De Sanctis M, Pastore C, Di Iaconi C (2018) Biomethanization of citrus waste: effect of waste characteristics and of storage on treatability and evaluation of limonene degradation. J Environ Manage 215:366–376. https://doi.org/10.1016/J.JENVMAN.2018.03.057
doi: 10.1016/J.JENVMAN.2018.03.057
pubmed: 29602026
Zema, D. A., Calabro, P. S., Folino, A., Tamburino, V., Zappia, G., &Zimbone, S. M. (2019, December 1). Wastewater management in citrus processing industries: An overview of advantages and limits. Water (Switzerland). MDPI AG. https://doi.org/10.3390/w11122481
Forgács G, Pourbafrani M, Niklasson C, Taherzadeh MJ, Hováth IS (2012) Methane production from citrus wastes: process development and cost estimation. J Chem Technol Biotechnol 87(2):250–255. https://doi.org/10.1002/jctb.2707
doi: 10.1002/jctb.2707
Wikandari R, Nguyen H, Millati R, Niklasson C, Taherzadeh MJ (2015) Improvement of biogas production from orange peel waste by leaching of limonene. Biomed Res Int 2015:494182. https://doi.org/10.1155/2015/494182
doi: 10.1155/2015/494182
pubmed: 25866787
pmcid: 4383308
Sokovicx M et al (2010) Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules 15(11):7532–7546. https://doi.org/10.3390/molecules15117532
doi: 10.3390/molecules15117532
Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3(7):408–414. https://doi.org/10.1038/nchembio.2007.5
doi: 10.1038/nchembio.2007.5
pubmed: 17576428
Tranchida PQ, Zoccali M, Bonaccorsi I, Dugo P, Mondello L, Dugo G (2013) The off-line combination of high-performance liquid chromatography and comprehensive two-dimensional gas chromatography-mass spectrometry: a powerful approach for highly detailed essential oil analysis. J Chromatogr A 1305:276–284. https://doi.org/10.1016/j.chroma.2013.07.042
doi: 10.1016/j.chroma.2013.07.042
pubmed: 23890548
Thomas AF, Bessière Y (1989) Limonene. Nat Prod Rep 6(3):291–309. https://doi.org/10.1039/NP9890600291
doi: 10.1039/NP9890600291
Guzmán J, Mosteo R, Sarasa J, Alba JA, Ovelleiro JL (2016) Evaluation of solar photo-Fenton and ozone-based processes as citrus wastewater pre-treatments. Sep Purif Technol 164:155–162. https://doi.org/10.1016/j.seppur.2016.03.025
doi: 10.1016/j.seppur.2016.03.025
Pourbafrani M, Forgács G, Horváth IS, Niklasson C, Taherzadeh MJ (2010) Production of biofuels, limonene and pectin from citrus wastes. Biores Technol 101(11):4246–4250. https://doi.org/10.1016/J.BIORTECH.2010.01.077
doi: 10.1016/J.BIORTECH.2010.01.077
Ponezi AN, Duarte MC, Filho BC, Figueiredo RF (2005) Analysis of biodegradation of citric oil compounds by GC/MSD and analysis of the microbial population of an activated sludge reactor in the treatment of a citric wastewater. Engenharia Sanitaria e Ambiental 10(4):278–284
doi: 10.1590/S1413-41522005000400003
Elnekave M, Celik SO, Tatlier M, Tufekci N (2012) Artificial neural network predictions of up-flow anaerobic sludge blanket (UASB) reactor performance in the treatment of citrus juice wastewater. Pol J Environ Stud 21(1):49–56
Marmulla R, Harder J (2014) Microbial monoterpene transformations-a review. Front Microbiol 5(JULY):346. https://doi.org/10.3389/fmicb.2014.00346
doi: 10.3389/fmicb.2014.00346
pubmed: 25076942
pmcid: 4097962
Rodrigues BCG, de Mello BS, da Silva BF, Pozzi E, de Lima Gomes PCF, Sarti A (2021) Limonene removal using a horizontal-flow anaerobic immobilized biomass bioreactor. J Water Process Eng 43:102225. https://doi.org/10.1016/j.jwpe.2021.102225
doi: 10.1016/j.jwpe.2021.102225
Ruiz, B., & Flotats, X. (2014). Citrus essential oils and their influence on the anaerobic digestion process: An overview. Waste Management. Elsevier Ltd. https://doi.org/10.1016/j.wasman.2014.06.026
Mizuki E, Akao T, Saruwatari T (1990) Inhibitory effect of Citrus unshu peel on anaerobic digestion. BiologicalWastes 33(3):161–168. https://doi.org/10.1016/0269-7483(90)90002-A
doi: 10.1016/0269-7483(90)90002-A
Dabbah R, Edwards VM, Moats WA (1970) Antimicrobial action of some citrus fruit oils on selected food-borne bacteria. Appl Microbiol 19(1):27–31. https://doi.org/10.1128/aem.19.1.27-31.1970
doi: 10.1128/aem.19.1.27-31.1970
pubmed: 4905947
pmcid: 376603
Erasto P, Viljoen AM (2008) Limonene—A review: biosynthetic, ecological and pharmacological relevance. Nat Prod Commun 3(7):1193–1202. https://doi.org/10.1177/1934578x0800300728
doi: 10.1177/1934578x0800300728
Chatterjee T, Bhattacharyya DK (2001) Biotransformation of limonene by Pseudomonas putida. Appl Microbiol Biotechnol 55(5):541–546. https://doi.org/10.1007/s002530000538
doi: 10.1007/s002530000538
pubmed: 11414318
di Pasqua R, Betts G, Hoskins N, Edwards M, Ercolini D, Mauriello G (2007) Membrane toxicity of antimicrobial compounds from essential oils. J Agric Food Chem 55(12):4863–4870. https://doi.org/10.1021/jf0636465
doi: 10.1021/jf0636465
pubmed: 17497876
Martins GS, Rodrigues T, Lamarca RS et al (2023) Continuous removal of caffeine in a horizontal-flow anaerobic immobilized biomass bioreactor: identification of transformation products. Environ Sci Pollut Res 30:107759–107771
doi: 10.1007/s11356-023-29875-x
Oliveira CA, Penteado ED, Tomita IN, Santos-Neto ÁJ, Zaiat M, da Silva BF, Lima Gomes PCF (2019) Removal kinetics of sulfamethazine and its transformation products formed during treatment using a horizontal flow-anaerobic immobilized biomass bioreactor. J Hazard Mater 365:34–43. https://doi.org/10.1016/J.JHAZMAT.2018.10.077
doi: 10.1016/J.JHAZMAT.2018.10.077
pubmed: 30408685
Rodriguez RP, Vich DV, Garcia ML, Varesche MBA, Zaiat M (2016) Application of horizontal-flow anaerobic immobilized biomass reactor for bioremediation of acid mine drainage. J Water Health 14(3):399–410. https://doi.org/10.2166/wh.2015.241
doi: 10.2166/wh.2015.241
pubmed: 27280606
Damianovic MHRZ, Moraes EM, Zaiat M, Foresti E (2009) Pentaclorofenol (PCP) dechlorination in horizontal-flow anaerobic immobilized biomass (HAIB) reactors. Bioresour Technol 100:4361–4367. https://doi.org/10.1016/j.biortech.2009.01.076
doi: 10.1016/j.biortech.2009.01.076
pubmed: 19443213
Zaiat M, Cabral AKA, Foresti E (1994) Horizontal-flow anaerobic immobilized sludge reactor for wastewater treatment:c conception and preliminary performance evaluation. Braz J Chem Eng 11(2):33–42
American Public Health Association (APHA) (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, Washington, DC, USA
Ripley, L. E., Boyle, W. C., & Converse, J. C. (1986). Improved alkalimetric monitoring for anaerobic digestion of high-strength wastes. Journal of the Water Pollution Control Federation, 58(5), 406–411. https://www.scopus.com/inward/record.uri?eid=2-s2.0-0022719568&partnerID=40&md5=65c67053b44c574e475e827d35f3810e
DiLallo R, Albertson OE (1961) Volatile acids by direct titration. Water Pollut Control Fed 33(4):356–365. https://doi.org/10.1073/pnas.0807060105
doi: 10.1073/pnas.0807060105
Camargo FP, Sarti A, Alécio AC, Sabatini CA, Tallarico Adorno MA, Silveira Duarte IC, Amâncio Varesche MB (2020) Limonene quantification by gas chromatography with mass spectrometry (gc-ms) and its effects on hydrogen and volatile fatty acids production in anaerobic reactors. Quimica Nova 43(7):844–850. https://doi.org/10.21577/0100-4042.20170557
doi: 10.21577/0100-4042.20170557
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303
doi: 10.1038/nmeth.f.303
pubmed: 20383131
pmcid: 3156573
Speece, R. E. (1983). Anaerobic biotechnology for industrial wastewater treatment. (J. M. Speece, Ed.) Environmental Science and Technology (1ST ed., Vol. 17). Nashiville: Archae Press. https://doi.org/10.1021/es00115a001
Srilatha HR, Nand K, Babu KS, Madhukara K (1995) Fungal pretreatment of orange processing waste by solid-state fermentation for improved production of methane. Process Biochem 30(4):327–331. https://doi.org/10.1016/0032-9592(95)87041-5
doi: 10.1016/0032-9592(95)87041-5
di Pasqua R, Hoskins N, Betts G, Mauriello G (2006) Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J Agric Food Chem 54(7):2745–2749. https://doi.org/10.1021/jf052722l
doi: 10.1021/jf052722l
pubmed: 16569070
Ultee A, Kets EPW, Alberda M, Hoekstra FA, Smid EJ (2000) Adaptation of the food-borne pathogen Bacillus cereus to carvacrol. Arch Microbiol 174(4):233–238. https://doi.org/10.1007/s002030000199
doi: 10.1007/s002030000199
pubmed: 11081791
Bakkali F, Averbeck S, Averbeck D, Idaomar M (2008) Biological effects of essential oils—A review. Food Chem Toxicol 46(2):446–475. https://doi.org/10.1016/j.fct.2007.09.106
doi: 10.1016/j.fct.2007.09.106
pubmed: 17996351
Eryildiz B et al (2020) Effect of pH, substrate loading, oxygen, and methanogens inhibitors on volatile fatty acid (VFA) production from citrus waste by anaerobic digestion. Bioresour Technol 302:122800. https://doi.org/10.1016/J.BIORTECH.2020.122800
doi: 10.1016/J.BIORTECH.2020.122800
pubmed: 31986336
Schink B (2002) Anaerobic digestion: concepts, limits and perspectives. Water Sci Technol: J Int Assoc Water Pollut Res 45(10):1–8. https://doi.org/10.2166/wst.2002.0274
doi: 10.2166/wst.2002.0274
Fuertes MBR, Patiño JDR, Vidal AP (2009) Effects of limonene on anaerobic co-digestion of citrus waste. Int Wissenschaftstagung Biogas Sci 3:485–490
Godon JJ, Morinière J, Moletta M, Gaillac M, Bru V, Delgènes JP (2005) Rarity associated with specific ecological niches in the bacterial world: the “Synergistes” example. Environ Microbiol 7(2):213–224. https://doi.org/10.1111/j.1462-2920.2004.00693.x
doi: 10.1111/j.1462-2920.2004.00693.x
pubmed: 15658988
del Nery V, de Nardi IR, Damianovic MHRZ, Pozzi E, Amorim AKB, Zaiat M (2007) Long-term operating performance of a poultry slaughterhouse wastewater treatment plant. Resour Conserv Recycl 50(1):102–114. https://doi.org/10.1016/J.RESCONREC.2006.06.001
doi: 10.1016/J.RESCONREC.2006.06.001
Militon C, Hamdi O, Michotey V, Fardeau ML, Ollivier B, Bouallagui H et al (2015) Ecological significance of Synergistetes in the biological treatment of tuna cooking wastewater by an anaerobic sequencing batch reactor. Environ Sci Pollut Res 22(22):18230–18238. https://doi.org/10.1007/s11356-015-4973-x
doi: 10.1007/s11356-015-4973-x
Yamashita T, Ishida M, Asakawa S, Kanamori H, Sasaki H, Ogino A et al (2016) Enhanced electrical power generation using flame-oxidized stainless steel anode in microbial fuel cells and the anodic community structure. Biotechnol Biofuels 9(1):1–10. https://doi.org/10.1186/s13068-016-0480-7
doi: 10.1186/s13068-016-0480-7
Yin Q, Miao J, Li B, Wu G (2017) Enhancing electron transfer by ferroferric oxide during the anaerobic treatment of synthetic wastewater with mixed organic carbon. Int Biodeterior Biodegradation 119:104–110. https://doi.org/10.1016/J.IBIOD.2016.09.023
doi: 10.1016/J.IBIOD.2016.09.023
Rotaru AE, Schauer R, Probian C, Mussmann M, Harder J (2012) Visualization of candidate division OP3 cocci in limonene-degrading methanogenic cultures. J Microbiol Biotechnol 22(4):457–461. https://doi.org/10.4014/jmb.1110.10055
doi: 10.4014/jmb.1110.10055
pubmed: 22534291
Motteran F, Braga JK, Silva EL, Varesche MBA (2016) Kinetics of methane production and biodegradation of linear alkylbenzene sulfonate from laundry wastewater. J Environ Sci Health—Part A Toxic/Hazardous Subst Environ Eng 51(14):1288–1302. https://doi.org/10.1080/10934529.2016.1215197
doi: 10.1080/10934529.2016.1215197
Harder J, Probian C (1995) Microbial degradation of monoterpenes in the absence of molecular oxygen. Appl Environ Microbiol 61(11):3804–3808. https://doi.org/10.1128/aem.61.11.3804-3808.1995
doi: 10.1128/aem.61.11.3804-3808.1995
pubmed: 8526489
pmcid: 167682
Förster-Fromme K, Höschle B, Mack C, Bott M, Armbruster W, Jendrossek D (2006) Identification of genes and proteins necessary for catabolism of acyclic terpenes and leucine/isovalerate in Pseudomonas aeruginosa. Appl Environ Microbiol 72(7):4819–4828. https://doi.org/10.1128/AEM.00853-06
doi: 10.1128/AEM.00853-06
pubmed: 16820476
pmcid: 1489323
Aissou M, Chemat-Djenni Z, Yara-Varón E, Fabiano-Tixier AS, Chemat F (2017) Limonene as an agro-chemical building block for the synthesis and extraction of bioactive compounds. ComptesRendus Chimie 20(4):346–358. https://doi.org/10.1016/J.CRCI.2016.05.018
doi: 10.1016/J.CRCI.2016.05.018
Bicas JL, Fontanille P, Pastore GM, Larroche C (2008) Characterization of monoterpene biotransformation in two pseudomonads. J Appl Microbiol 105(6):1991–2001. https://doi.org/10.1111/j.1365-2672.2008.03923.x
doi: 10.1111/j.1365-2672.2008.03923.x
pubmed: 19120646
Wackett LP (2003) Pseudomonas putida—A versatilebiocatalyst. Nat Biotechnol 21(2):136–138. https://doi.org/10.1038/nbt0203-136
doi: 10.1038/nbt0203-136
pubmed: 12560839
Madigan, M. T., Martinko, J. M., & Parker, J. (2015). Brock biology of micro-organisms (Vol. 11). Pearson Prentice Hall Upper Saddle River, NJ.
Wauven CV, Pierard A, Kley-Raymann M, Haas D (1984) Pseudomonas aeruginosa mutants affected in anaerobic growth on arginine: evidence for a four-gene cluster encoding the arginine deiminase pathway. J Bacteriol 160(3):918–934. https://doi.org/10.1128/jb.160.3.928-934.1984
doi: 10.1128/jb.160.3.928-934.1984
Calabrò PS, Pontoni L, Porqueddu I, Greco R, Pirozzi F, Malpei F (2016) Effect of the concentration of essential oil on orange peel waste biomethanization: preliminary batch results. Waste Manage 48:440–447. https://doi.org/10.1016/j.wasman.2015.10.032
doi: 10.1016/j.wasman.2015.10.032
Yoo SK, Day DF (2002) Bacterial metabolism of α- and β-pinene and related monoterpenes by Pseudomonas sp. strain PIN. Process Biochem 37(7):739–745. https://doi.org/10.1016/S0032-9592(01)00262-X
doi: 10.1016/S0032-9592(01)00262-X
Eaton RW (1997) p-cymene catabolic pathway in Pseudomonas putida F1: cloning and characterization of DNA encoding conversion of p-cymene to p-cumate. J Bacteriol 179(10):3171–3180. https://doi.org/10.1128/jb.179.10.3171-3180.1997
doi: 10.1128/jb.179.10.3171-3180.1997
pubmed: 9150211
pmcid: 179094
Mirzaie S, Rafii F, Yasunaga K, Yoshunaga K, Sepehrizadeh Z, Kanno S et al (2012) Prediction of the mode of interaction between monoterpenes and the nitroreductase from Enterobacter cloacae by docking simulation. Comput Biol Med 42(4):414–421. https://doi.org/10.1016/j.compbiomed.2011.12.009
doi: 10.1016/j.compbiomed.2011.12.009
pubmed: 22240115
Cole ER, dos Santos RB, Lacerda Júnior V, Martins JDL, Greco SJ, Cunha Neto A (2014) Chemical composition of essential oil from ripe fruit of Schinus terebinthifolius Raddi and evaluation of its activity against wild strains of hospital origin. Braz J Microbiol 45(3):821–828. https://doi.org/10.1590/S1517-83822014000300009
doi: 10.1590/S1517-83822014000300009
pubmed: 25477913
pmcid: 4204964
Gengde H, Zhenjie J, Sixu C, Liqiang Z, Zhicheng CAI, Ziqi LIN et al (2019) Effect of D-limonene nanoemulsion against foodborne pathogens in raw beef. J Agric Sci Technol 21(5):121
Park YJ, Kim IC, Chang HC (2003) Microbial conversion of (+)-limonene by an Enterobacter agglomerans isolate. J Microbiol Biotechnol 13(4):636–639
Yang EJ, Park YJ, Chang HC (2007) Cloning of four genes involved in limonene hydroxylation from Enterobacter cowanii 6L. J Microbiol Biotechnol 17(7):1169–1176
pubmed: 18051329
Azman S, Khadem AF, van Lier JB, Zeeman G, Plugge CM (2015) Presence and role of anaerobic hydrolytic microbes in conversion of lignocellulosic biomass for biogas production. Crit Rev Environ Sci Technol 45(23):2523–2564. https://doi.org/10.1080/10643389.2015.1053727
doi: 10.1080/10643389.2015.1053727
Rivière D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J et al (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J 3(6):700–714. https://doi.org/10.1038/ismej.2009.2
doi: 10.1038/ismej.2009.2
pubmed: 19242531
Nelson MC, Morrison M, Yu Z (2011) A meta-analysis of the microbial diversity observed in anaerobic digesters. Biores Technol 102(4):3730–3739. https://doi.org/10.1016/J.BIORTECH.2010.11.119
doi: 10.1016/J.BIORTECH.2010.11.119
McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B et al (2008) Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci 1125(1):58–72. https://doi.org/10.1196/annals.1419.005
doi: 10.1196/annals.1419.005
pubmed: 18378587
Ludwig W, Schleifer K-H, Whitman WB (2009) Taxonomic outline of the phylum Firmicutes. In: de Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA et al (eds) Systematic Bacteriology. Springer, New York, pp 15–17
doi: 10.1007/978-0-387-68489-5_2
Yamada T, Imachi H, Ohashi A, Harada H, Hanada S, Kamagata Y, Sekiguchi Y (2007) Bellilineacaldifistulae gen. nov., sp. nov and Longilineaarvoryzae gen. nov., sp. nov., strictly anaerobic, filamentous bacteria of the phylum Chloroflexi isolated from methanogenic propionate-degrading consortia. Int J Syst Evol Microbiol 57(10):2299–2306. https://doi.org/10.1099/ijs.0.65098-0
doi: 10.1099/ijs.0.65098-0
pubmed: 17911301
Björnsson L, Hugenholtz P, Tyson GW, Blackall LL (2002) Filamentous Chloroflexi (green non-sulfur bacteria) are abundant in wastewater treatment processes with biological nutrient removal c cThe EMBL accession numbers for the sequences reported in this paper are X84472 (strain SBR1029 16S rDNA), X84474 strain. Microbiology 148(8):2309–2318. https://doi.org/10.1099/00221287-148-8-2309
doi: 10.1099/00221287-148-8-2309
pubmed: 12177325
Gupta RS, Lo B, Son J (2018) Phylogenomics and comparative genomic studies robustly support division of the genus Mycobacterium into an emended genus Mycobacterium and four novel genera. Front Microbiol. https://doi.org/10.3389/fmicb.2018.00067
doi: 10.3389/fmicb.2018.00067
pubmed: 30700981
pmcid: 6297179