Abstract
Oily bilge wastewater (OBW) is a hazardous hydrocarbon-waste generated by ships worldwide. In this research, we enriched, characterized and study the hydrocarbon biodegradation potential of a microbial consortium from the bilges of maritime ships. The consortium cZ presented a biodegradation efficiency of 66.65% for total petroleum hydrocarbons, 72.33% for aromatics and 97.76% removal of n-alkanes. This consortium showed the ability to grow in OBWs of diverse origin and concentration. A 67-fold increase in biomass was achieved using a Sequential Batch Reactor with OBW as the only carbon and energy source. The bacterial community composition of the enriched OBW bacterial consortium at the final stable stage was characterized by 16S amplicon Illumina sequencing showing that 25 out of 915 of the emerged predominant bacterial types detected summed up for 84% of total composition. Out of the 140 taxa detected, 13 alone accumulated 94.9% of the reads and were classified as Marinobacter, Alcanivorax, Parvibaculum, Flavobacteriaceae, Gammaproteobacteria PYR10d3, Novispirillum and Xanthomonadaceae among the most predominant, followed by Thalassospira, Shewanella, Rhodospirillaceae, Gammaprotobacteria, Rhodobacteriaceae and Achromobacter. The microbial community from OBW bioreactor enrichments is intrinsically diverse with clear selection of predominant types and remarkably exhibiting consistent and efficient biodegradation achieved without any nutrient or surfactant addition. Due to there is very little information available in the OBW biodegradation field, this work contributes to the body of knowledge surrounding the treatment improvement of this toxic waste and its potential application in wastewater management.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
European Nucleotide Archive, accession number: PRJEB36985.
Code availability
Not applicable.
References
Abraham WR, Meyer H, Yakimov M (1998) Novel glycine containing glucolipids from the alkane using bacterium Alcanivorax borkumensis. Biochim Biophys Acta 1393:57–62. https://doi.org/10.1016/s0005-2760(98)00058-7
An D, Caffrey SM, Soh J et al (2013) Metagenomics of hydrocarbon resource environments indicates aerobic taxa and genes to be unexpectedly common. Environ Sci Technol 47:10708–10717. https://doi.org/10.1021/es4020184
APHA, AWWA, WEF (1998) Standard Method for the examination of Wastewater., Franson, M. American Public Health Association, Washington DC
ASTM Standard D4928 (2012) Standard test method for water in crude oils by coulometric Karl Fischer titritation
ASTM Standard D7678 (2011) Standard test method for total petroleum hydrocarbons (TPH) in water and wastewater with solvent extraction using Mid-IR laser spectroscopy
ASTM Standard D854 (2014) Standard test methods for specific gravity of soils solids by water pycnometer
ASTM Standard D88-07 (1999) Standard test methods for saybolt viscocity
Atlas RM (1981) Microbial degradation of petroleum hydrocarbons: an environmental perspective. Microbiol Rev 45:180–209
Atlas RM (1988) Microbiology: fundamentals and applications, 2nd edn. University of Michigan, Ann Arbor
Atlas RM, Uterman R (2002) Bioremediation. Manual of environmental microbiology. ASM Press, Washington DC, pp 666–681
Batista SB, Mounteer AH, Amorim FR, Tótola MR (2006) Isolation and characterization of biosurfactant/bioemulsifier-producing bacteria from petroleum contaminated sites. Bioresour Technol 97:868–875. https://doi.org/10.1016/j.biortech.2005.04.020
Cai L, Rensing C, Li X, Wang G (2009) Novel gene clusters involved in arsenite oxidation and resistance in two arsenite oxidizers: Achromobacter sp. SY8 and Pseudomonas sp. TS44. Appl Microbiol Biotechnol 83(4):715–725
Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high- throughput community sequencing data intensity normalization improves color calling in SOLiD sequencing. Nat Methods 7:335–433. https://doi.org/10.1038/nmeth.f.303
Cerqueira VS, Hollenbach EB, Maboni F et al (2011) Biodegradation potential of oily sludge by pure and mixed bacterial cultures. Bioresour Technol 102:11003–11010. https://doi.org/10.1016/j.biortech.2011.09.074
Chai L, Wang Y, Yang Z, Wang Q, Wang H (2010) Detoxification of chromium-containing slag by Achromobacter sp. CH-1 and selective recovery of chromium. Trans Nonfer Metals Soc China 20(8):1500–1504
Chaudhary DK, Kim J (2018) Flavobacterium naphthae sp. nov., isolated from oil-contaminated soil. Int J Syst Evol Microbiol 68:305–309. https://doi.org/10.1099/ijsem.0.002504
Clark DS, Blanch HW (1997) Biochemical engineering, 2nd edn. CRC Press, New York
Corti Monzón G, Nisenbaum M, Herrera Seitz MK, Murialdo SE (2018) New findings on aromatic compounds’ degradation and their metabolic pathways, the biosurfactant production and motility of the Halophilic Bacterium Halomonas sp. KHS3. Curr Microbiol 75:1108–1118. https://doi.org/10.1007/s00284-018-1497-x
Cui Z, Gao W, Xu G et al (2016) Marinobacter aromaticivorans sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from sea sediment. Int J Syst Evol Microbiol 66:353–359. https://doi.org/10.1099/ijsem.0.000722
Das R, Kazy SK (2014) Microbial diversity, community composition and metabolic potential in hydrocarbon contaminated oily sludge: prospects for in situ bioremediation. Environ Sci Pollut Res 21:7369–7389. https://doi.org/10.1007/s11356-014-2640-2
Dashti N, Ali N, Salamah S et al (2019) Culture-independent analysis of hydrocarbonoclastic bacterial communities in environmental samples during oil: bioremediation. Microbiologyopen 8:e630. https://doi.org/10.1002/mbo3.630
Dastgheib SMM, Amoozegar MA, Khajeh K et al (2012) Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol 95:789–798. https://doi.org/10.1007/s00253-011-3706-4
Deng M-C, Li J, Liang F-R et al (2014) Isolation and characterization of a novel hydrocarbon-degrading bacterium Achromobacter sp. HZ01 from the crude oil-contaminated seawater at the Daya Bay, southern China. Mar Pollut Bull 83:79–86. https://doi.org/10.1016/j.marpolbul.2014.04.018
Deng W, De Hoog CL, Yu HB et al (2010) A comprehensive proteomic analysis of the type III secretome of Citrobacter rodentium. J Biol Chem 285:6790–6800. https://doi.org/10.1074/jbc.M109.086603
Di Bella G, Di Prima N, Di Tapani D et al (2015) Performance of membrane bioreactor (MBR) systems for the treatment of shipboard slops: assessment of hydrocarbon biodegradation and biomass activity under salinity variation. J Hazard Mater 300:765–778. https://doi.org/10.1016/j.jhazmat.2015.08.021
Eckford R, Cook FD, Saul D et al (2002) Free-living heterotrophic nitrogen-fixing bacteria isolated from fuel-contaminated antarctic soils. Appl Environ Microbiol 68:5181–5185. https://doi.org/10.1128/AEM.68.10.5181
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
Emadian SM, Hosseini M, Rahimnejad M et al (2015) Treatment of a low-strength bilge water of Caspian Sea ships by HUASB technique. Ecol Eng 82:272–275. https://doi.org/10.1016/j.ecoleng.2015.04.055
EPA-821-R-98-002 (1999) Method 1664, revision A: n-hexane extractable material (HEM; Oil and Grease) and silica gel treated n-hexane extractable material (SGT—HEM; non-polar material) by extraction and gravimetry. EPA-821-R-98-002, Washington DC
EPA-833-F-11-001 (2011) Vessel general permit (VGP) for discharges incidental to the normal operation of vessels. EPA-833-F-11-001, Washington DC
EPA833-R-10-005 (2010) Report to congress: study of discharges incidental to normal operation of commercial fishing vessels and other non recreational vessels less than 79 ft. EPA833-R-10-005, Washington, DC
EPA842-R-07-005 (2008) Cruise ship discharge assessment report. Section 4: Oily Bilge Water. EPA842-R-07-005, Washington DC
EPA842-R-99-001 (1999) Phase I final rule and technical development document of uniform national discharge standards (UNDS). Appendix A. EPA842-R-99-001, Washington DC
Fan X, Yu T, Li Z, Zhang X (2019) Luteimonas abyssi sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 64:668–674. https://doi.org/10.1099/ijs.0.056010-0
Finney BYDJ (1951) The estimation of bacterial densities from dilution series. J Hyg 49:26–35
Fowler SJ, Toth CRA, Gieg LM (2016) Community structure in methanogenic enrichments provides insight into syntrophic interactions in hydrocarbon-impacted environments. Front Microbiol 7:1–13. https://doi.org/10.3389/fmicb.2016.00562
Frysinger GS, Gaines RB, Xu L, Reddy CM (2003) Resolving the unresolved complex mixture in petroleum-contaminated sediments. Environ Sci Technol 37:1653–1662. https://doi.org/10.1021/es020742n
Furukawa K (2000) Biochemical and genetic bases of microbial degradation of polychlorinated biphenyls (PCBs). J Gen Appl Microbiol 46(6):283–296
García-Bonilla E, Brandão PF, Pérez T, Junca H (2019) Stable and enriched Cenarchaeum symbiosum and uncultured Betaproteobacteria HF1 in the microbiome of the Mediterranean Sponge Haliclonafulva (Demospongiae: Haplosclerida). Microb Ecol 77:25–36
Gauthier MJ, Lafay B, Christen R et al (1992) Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 42:568–576
Geerdink MJ, van Loosdrecht MCM, Luyben KCAM (1996) Biodegradability of diesel oil. Biodegradation 7:73–81. https://doi.org/10.1007/BF00056560
Giebel H-A, Klotz F, Voget S et al (2016) Draft genome sequence of the marine Rhodobacteraceae strain O.365, cultivated from oil-polluted seawater of the Deepwater Horizon oil spill. Stand Genomic Sci 11:81
Gomila M, Tvrzova L, Teshim A et al (2011) Achromobacter marplatensis sp. nov., isolated from a pentachlorophenol-contaminated soil. Int J Syst Evol Microbiol 61:2231–2237. https://doi.org/10.1099/ijs.0.025304-0
Gouveia V, Almeida CMR, Almeida T et al (2018) Indigenous microbial communities along the NW Portuguese Coast : Potential for hydrocarbons degradation and relation with sediment contamination. Mar Pollut Bull 131:620–632. https://doi.org/10.1016/j.marpolbul.2018.04.063
Green DH, Bowman JP, Smith EA et al (2006) Marinobacter algicola sp. nov., isolated from laboratory cultures of paralytic shellfish toxin- producing dinoflagellates. Int J Syst Evol Microbiol 56:523–527. https://doi.org/10.1099/ijs.0.63447-0
Gunkel W (1968) Bacteriological investigations of oil-polluted sedimens from the Cornich Coast following the “Torrey canyon’’ disaster. In: Carthy JD, Arthur DR (eds) The biological effects of oil pollution on littoral communities. Classey E.W. Ltd., Hampton, pp 151–158
Handley KM, Lloyd JR (2013) Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species. Front Microbiol 4:1–10. https://doi.org/10.3389/fmicb.2013.00136
Hara A, Syutsubo K, Harayama S (2003) Alcanivorax which prevails in oil-contaminated seawater exhibits broad substrate specificity for alkane degradation. Environ Microbiol 5:746–753. https://doi.org/10.1046/j.1462-2920.2003.00468.x
Head IM, Gray ND, Larter SR (2014) Life in the slow lane; biogeochemistry of biodegraded petroleum containing reservoirs and implications for energy recovery and carbon management. Front Microbiol 5:566. https://doi.org/10.3389/fmicb.2014.00566
Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182. https://doi.org/10.1038/nrmicro1348
Hedlund BP, Geiselbrecht AD, Staley JT (2001) Marinobacter strain NCE312 has a Pseudomonas-like naphthalene dioxygenase. FEMS Microbiol Lett 201:47–51
Hu G, Li J, Zeng G (2013) Recent development in the treatment of oily sludge from petroleum industry: a review. J Hazard Mater 261:470–490. https://doi.org/10.1016/j.jhazmat.2013.07.069
Huang H, Yu H, Qi M et al (2019) Enrichment and characterization of a highly efficient tetrahydrofuran-degrading bacterial culture. Biodegradation. https://doi.org/10.1007/s10532-019-09888-5
IMO (1988) International convention for the prevention of pollution from ships (MARPOL). Annex V Prevention of Pollution by Garbage from Ships
Janbandhu A, Fulekar MH (2011) Biodegradation of phenanthrene using adapted microbial consortium isolated from petrochemical contaminated environment. J Hazard Mater 187:333–340. https://doi.org/10.1016/j.jhazmat.2011.01.034
Jencova V, Strnad H, Chodora Z et al (2008) Nucleotide sequence, organization and characterization of the (halo)aromatic acid catabolic plasmid pA81 from Achromobacter xylosoxidans A8. Res Microbiol 159:118–127. https://doi.org/10.1016/j.resmic.2007.11.018
Jooste PJ, Hugo CJ (1999) The taxonomy, ecology and cultivation of bacterial genera belonging to the family Flavobacteriaceae. Int Journl Food Microbiol 53:81–94. https://doi.org/10.1016/S0168-1605(99)00162-2
Kerkhoff MJ, Files LA, Winefordner JD (1985) Identification of polyaromatic hydrocarbon mixtures by low-temperature constant energy synchronous fluorescence spectrometry. AnalChem 57:1673–1676
Kodama Y, Stiknowati LI, Ueki A et al (2008) Thalassospira tepidiphilaomatic sp. nov., a polycyclic Ar hydrocarbon-degrading bacterium isolated from seawater. Int J Syst Evol Microbiol 58:711–715. https://doi.org/10.1099/ijs.0.65476-0
Kostka JE, Prakash O, Overholt WA et al (2011) Hydrocarbon-degrading bacteria and the bacterial community response in gulf of mexico beach sands impacted by the deepwater horizon oil spill. Appl Environ Microbiol 77:7962–7974. https://doi.org/10.1128/AEM.05402-11
Krell T (2018) Cellular Ecophysiology of microbe: hydrocarbon and lipid interactions, 1st edn. Springer, New York
Kumar BL, Gopal DVRS (2015) Effective role of indigenous microorganisms for sustainable environment. 3 Biotech 5:867–876. https://doi.org/10.1007/s13205-015-0293-6
Lamendella R, Strutt S, Borglin S et al (2014) Assessment of the Deepwater Horizon oil spill impact on Gulf coast microbial communities. Front Microbiol 5:130. https://doi.org/10.3389/fmicb.2014.00130
Liu L, Liu Y, Lin J et al (2007) Development of analytical methods for polycyclic aromatic hydrocarbons (PAHs) in airborne particulates: a review. J Environ Sci 19:1–11. https://doi.org/10.1016/S1001-0742(07)60001-1
Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P (1992) A new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 42:568–576
Mahjoubi M, Jaouani A, Guesmi A et al (2013) Hydrocarbonoclastic bacteria isolated from petroleum contaminated sites In Tunisia: Isolation, identification and characterization of the biotechnological potential. Biotechnology 30:723–733. https://doi.org/10.1016/j.nbt.2013.03.004
Mancini G, Cappello S, Yakimov M (2012) Biological approaches to the treatment of saline oily waste (waters) originated from marine transportation. Chemistry 27:37–42
Marchal R, Penet S, Vandecasteele JP (2003) Gasoline and diesel oil biodegradation. Oil Gas Sci Technol 58:441–448
Margareth E, Brito S, Guyoneaud RR et al (2006) Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara Bay, Brazil. Res Microbiol 157:752–762. https://doi.org/10.1016/j.resmic.2006.03.005
Marín M, Pedregosa A, Ríos S et al (1995) Biodegradation of diesel and heating oil by Acinetobacter calcoaceticus MM5: its possible applications on bioremediation. Int Biodeterior Biodegrad 35:269–285. https://doi.org/10.1016/0964-8305(95)00067-F
McBride MJ (2014) The family Flavobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, et al. (eds) The prokaryotes: other major lineages of bacteria and the archaea. Springer, Berlin, pp 643–676
McLaughlin C, Falatko D, Danesi R, Albert R (2014) Characterizing shipboard bilgewater effluent before and after treatment. Environ Sci Pollut Res 21:5637–5652. https://doi.org/10.1007/s11356-013-2443-x
Meredith W, Kelland SJ, Jones DM (2000) Influence of biodegradation on crude oil acidity and carboxylic acid composition. Org Geochem 31(11):1059–1073
Militon C, Boucher D, Vachelard C et al (2010) Bacterial community changes during bioremediation of aliphatic hydrocarbon-contaminated soil. FEMS Microbiol Ecol 74:669–681. https://doi.org/10.1111/j.1574-6941.2010.00982.x
Moreno-Andrade I, Buitrón G (2012) Comparison of the performance of membrane and conventional sequencing batch reactors degrading 4-chlorophenol. Water Air Soil Pollut 223:2083–2091. https://doi.org/10.1007/s11270-011-1006-3
Murialdo SE, Fenoglio R, Haure PM, González JF (2003) Degradation of phenol and chlorophenols by mixed and pure cultures. WaterSA 29:457–464
Nievas ML, Commendatore MG, Esteves JL, Bucalá V (2005) Effect of pH modification on bilge waste biodegradation by a native microbial community. Int Biodeterior Biodegrad 56:151–157. https://doi.org/10.1016/j.ibiod.2005.06.006
Nievas ML, Commendatore MG, Esteves JL, Bucalá V (2008) Biodegradation pattern of hydrocarbons from a fuel oil-type complex residue by an emulsifier-producing microbial consortium. J Hazard Mater 154:96–104. https://doi.org/10.1016/j.jhazmat.2007.09.112
Nievas ML, Commendatore MG, Olivera NL et al (2006) Biodegradation of bilge waste from Patagonia with an indigenous microbial community. Bioresour Technol 97:2280–2290. https://doi.org/10.1016/j.biortech.2005.10.042
Nisenbaum M, Sendra GH, Cerdá Gilbert GA et al (2013) Hydrocarbon biodegradation and dynamic laser speckle for detecting chemotactic responses at low bacterial concentration. J Environ Sci 25:613–625. https://doi.org/10.1016/S1001-0742(12)60020-5
Olivera NL, Commendatore MG, Esteves JL, Delgado O (2003) Microbial characterization and hydrocarbon biodegradation potential of natural bilge waste microflora. J Ind Microbiol Biotechnol 30:542–548. https://doi.org/10.1007/s10295-003-0078-5
Païssé S, Goñi-urriza M, Coulon F, Duran R (2010) How a bacterial community originating from a contaminated coastal sediment responds to an oil input. Environ Microbiol 60:394–405. https://doi.org/10.1007/s00248-010-9721-7
Paixão DAA, Dimitrov MR, Pereira RM et al (2010) Molecular analysis of the bacterial diversity in a specialized consortium for diesel oil degradation. Rev Bras Ciênc Solo 34:773–781. https://doi.org/10.1590/S0100-06832010000300019
Palleroni NJ, Pieper DH, Moore ERB (2010) Microbiology of hydrocarbon-degrading pseudomonas. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin
Penet S, Marchal R, Sghir A, Monot F (2004) Biodegradation of hydrocarbon cuts used for diesel oil formulation. Appl Microbiol Biotechnol 66:40–47. https://doi.org/10.1007/s00253-004-1660-0
Pucci GN, Acuña AJ, Llanes ML et al (2009) Identificación de bacterias marinas cultivables de la ciudad costera Comodoro Rivadavia, Argentina. Rev Biol Mar Oceanogr 44:49–58. https://doi.org/10.4067/S0718-19572009000100005
Rahman KSM, Vasudevan N, Lakshmanaperumalsamy P (1999) Enhancement of biosurfactant production to emulsify different hydrocarbons. J Environ Poll 6:87–93
Rahman KSM, Rahman TJ, Kourkoutas Y et al (2003) Enhanced bioremediation of n-alkane in petroleum sludge using bacterial consortium amended with rhamnolipid and micronutrients. Bioresour Technol 90:159–168. https://doi.org/10.1016/S0960-8524(03)00114-7
Rahman KSM, Thahira-Rahman J, Lakshmanaperumalsamy P, Banat IM (2002) Towards efficient crude oil degradation by a mixed bacterial consortium. Bioresour Technol 85:257–261. https://doi.org/10.1016/S0960-8524(02)00119-0
Rehmann K, Hertkorn N, Kettrup AA (2001) Fluoranthene metabolism in Mycobacterium sp. strain KR20: identity of pathway intermediates during degradation and growth. Microbiology 147:2783–2794. https://doi.org/10.1099/00221287-147-10-2783
Rochman FF (2016) Aerobic hydrocarbon-degrading microbial communities in oilsands tailings ponds. University of Calgary, Calgary
Rosario-Passapera R, Keddis R, Wong R et al (2012) Parvibaculum hydrocarboniclasticum sp. nov., a isolated from a deep-sea hydrothermal vent on the East Pacific Rise. Int J Syst Evol Microbiol 62:2921–2926. https://doi.org/10.1099/ijs.0.039594-0
Rosenberg E, Legmann R, Kushmaro A et al (1992) Petroleum bioremediation: a multiphase problem. Biodegradation 3:337–350. https://doi.org/10.1007/BF00129092
Roy AS, Baruah R, Borah M et al (2014) Bioremediation potential of native hydrocarbon degrading bacterial strains in crude oil contaminated soil under microcosm study. Int Biodeterior Biodegrad. https://doi.org/10.1016/j.ibiod.2014.03.024
Salmon C, Crabos JL, Sambuco JP et al (1998) Artificial wetland performances in the purification efficiency of hydrocarbon wastewater. Water Air Soil Pollut 104:313–329. https://doi.org/10.1023/A:100492800
Santisi S, Gentile G, Volta A et al (2015) Isolation and characterization of oil- degrading bacteria from bilge water. Int J Microbiol Appl 2:45–49
Sarkar J, Kazy SK, Gupta A et al (2016) Biostimulation of indigenous microbial community for bioremediation of petroleum refinery sludge. Front Microbiol 7:1–20. https://doi.org/10.3389/fmicb.2016.01407
Schleheck D, Tindall BJ, Rosselló-Mora R, Cook AM (2004) Parvibaculum lavamentivorans gen. nov., sp. nov., a novel heterotroph that initiates catabolism of linear alkylbenzenesulfonate. Int J Syst Evol Microbiol 54:1489–1497. https://doi.org/10.1099/ijs.0.03020-0
Shivaji S, Gupta P, Chaturvedi P et al (2005) Marinobacter maritimus sp. nov., a psychrotolerant strain isolated from sea water off the subantarctic Kerguelen islands. Int J Syst Evol Microbiol 55:1453–1456. https://doi.org/10.1099/ijs.0.63478-0
Singer ME, Finnerty WR (1984) Microbial metabolism of straight-chain and branched alkanes. In: Atlas RM (ed) Petroleum microbiology. Macmillan, New York, pp 1–59
Singleton DR, Sangaiah R, Gold A et al (2006) Identification and quantification of uncultivated proteobacteria associated with pyrene degradation in a bioreactor treating PAH-contaminated soil. Environ Microbiol 8:1736–1745. https://doi.org/10.1111/j.1462-2920.2006.01112.x
Sivaraman C, Ganguly A, Nikolausz M, Mutnuri S (2011) Isolation of hydrocarbonoclastic bacteria from bilge oil contaminated water. Int J Environ Sci Technol 8:461–470. https://doi.org/10.1007/BF03326232
Smith JR, Nakles DV, Sherman DF, Neuhauser EF, Loehr RC (1989) Environmental fate mechanism infuencing biological degradation of coal-tar derived polynuclear aromatic hydrocarbons in soil systems. Third international conference on new frontiers for hazardous waste management. US Environmental Protection Agency, Washington, DC, pp 397–405
Stanbury PF, Whitaker A, Hall SJ (2016) Principles of Fermentation technology, 3rd edn. Elsevier, Amsterdam
Sun C, Leiknes TO, Weitzenböck J, Thorstensen B (2009) The effect of bilge water on a Biofilm—MBR process in an integrated shipboard wastewater treatment system. Desalination 236:56–64. https://doi.org/10.1016/j.desal.2007.10.051
Takai K, Moyer CL, Miyazaki M et al (2005) Marinobacter alkaliphilus sp. nov., a novel alkaliphilic bacterium isolated from subseafloor alkaline serpentine mud from Ocean Drilling Program Site 1200 at South Chamorro Seamount. Mar Forearc Extremophiles 9:17–27. https://doi.org/10.1007/s00792-004-0416-1
Techtmann SM, Hazen TC (2016) Metagenomic applications in environmental monitoring and bioremediation. J Ind Microbiol Biotechnol 43:1345–1354. https://doi.org/10.1007/s10295-016-1809-8
Timmis KN (2010) Handbook of Hydrocarbon and Lipid Microbiology, Timmis K. Springer, Berlin/Heidelberg
Tiselius P, Magnusson K (2017) Toxicity of treated bilge water: The need for revised regulatory control. Mar Pollut Bull 114:860–866. https://doi.org/10.1016/j.marpolbul.2016.11.010
Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286. https://doi.org/10.1016/j.biortech.2016.10.037
Vestal R, Cooney JJ, Crow S, Berger J (1984) The effects of hydrocarbons on aquatic microorganisms. In: Macmillan (ed) Petroleum Microbiology. New York, pp 475–505
Viñas M, Solanas A (2005) Biorremediación de suelos contaminados por hidrocarburos: caracterización microbiológica, química y ecotoxicológica
Vyrides I, Drakou EM, Ioannou S et al (2018) Biodegradation of bilge water: Batch test under anaerobic and aerobic conditions and performance of three pilot aerobic Moving Bed Biofilm Reactors (MBBRs) at different filling fractions. J Environ Manage 217:356–362. https://doi.org/10.1016/j.jenvman.2018.03.086
Wakeham SG (1977) Synchronous fluorescence spectroscopy and its application to indigenous and petroleum-derived hydrocarbons in lacustrine sediments. Environ Sci Technol 11:272–276. https://doi.org/10.1021/es60126a012
Walters W, Hyde ER, Berg-Lyons D et al (2016) Improved bacterial 16S rRNA Gene (V4 and V4–5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems. https://doi.org/10.1128/mSystems.00009-15
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.000625.2.1
Wang Y, Wang Q, Li M et al (2016) An alternative anaerobic treatment process for treatment of heavy oil refinery wastewater containing polar organics. Biochem Eng J 105:44–51. https://doi.org/10.1016/j.bej.2015.08.012
Warr LN, Schlüter M, Schauer F et al (2018) Applied Clay Science Nontronite-enhanced biodegradation of Deepwater Horizon crude oil by Alcanivorax borkumensis. Appl Clay Sci 158:11–20. https://doi.org/10.1016/j.clay.2018.03.011
Wojcieszyńska D, Hupert-Kocurek K, Greń I, Guzik U (2011) High activity catechol 2,3-dioxygenase from the cresols: degrading Stenotrophomonas maltophilia strain KB2. Int Biodeterior Biodegrad 65:853–858. https://doi.org/10.1016/j.ibiod.2011.06.006
Yang S, Wen X, Zhao L et al (2014) Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia Crude Oil Pipeline route. PLoS ONE 9:e96552. https://doi.org/10.1371/journal.pone.0096552
Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS ONE 7:e30058. https://doi.org/10.1371/journal.pone.0030058
Youssef M (2010) Hydrocarbon degrading bacteria as indicator of petroleum pollution in Ismailia Canal. Egypt Pollut Res 8:1226–1233
YPF (2014) Diesel 500. Ficha tecnica Nro 21.
YPF (2012) Fuel oil marino RME 180, Ficha tecnica Nro15
Zhao B, Wang H, Li R, Mao X (2010) Thalassospira xianhensis sp. nov., a polycyclic aromatic hydrocarbon-degrading marine bacterium. Int J Syst Evol Microbiol 60:1125–1129. https://doi.org/10.1099/ijs.0.013201-0
Acknowledgements
We would like to thank to Laboratorio de Análisis Fares Taie (www.farestaie.com.ar) for facilitating and conducting the laboratory analysis of OBW samples collected on this study. We also thank the collaboration of Dr. Enrique Ros, from the Universidad Nacional de la Patagonia San Juan Bosco, and Dr. Ignacio Durruty, from Universidad Nacional de Mar del Plata for their advice. H. Junca would like to thank Dr. Erika García-Bonilla (Microbiomas Foundation) and Dr. Ericsson Coy-Barreras (InquiBio, UMNG) for excellent scientific and infrastructure support and to Armando Junca and Rosa Peinado for financial support (Escuela para amar el agua). We also would like to thank the financial support from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC) and Universidad Nacional de Mar del Plata for reaserchers salaries and grants.
Funding
This project was supported partially by VT38-UNMdP10982, PIT-AP-BA-2016, PICT 2014-1567, CIC Ideas-Proyecto de Investigación en Temas Prioritarios y de Impacto Para la Provincia de Buenos Aires Res. Nº 801/18.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by MN, GC, MV, AM and MLP. Supervision was performed by SEM, HJ, and JFG. The first draft of the manuscript was written by MN and all authors commented on previous versions of the manuscript.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare that they have no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
All authors agreed with the content and that all gave explicit consent to submit this publication and they obtained consent from the responsible authorities at the institute/organization where the work has been carried out.
Consent for publication
All the authors approved the final version to be published.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10532_2020_9896_MOESM1_ESM.xls
Supplementary file1 (XLS 162 kb). EMS 1 Table including OTUs ID, classification, relative frequencies and corresponding representative sequences of all the OTUs determined in the microbial consortium
10532_2020_9896_MOESM2_ESM.docx
Supplementary file2 (DOCX 33 kb). EMS 2 Metabolic characteristics putatively associated to the predominant bacterial taxa detected in OBW degrading consortium
Rights and permissions
About this article
Cite this article
Nisenbaum, M., Corti-Monzón, G., Villegas-Plazas, M. et al. Enrichment and key features of a robust and consistent indigenous marine-cognate microbial consortium growing on oily bilge wastewaters. Biodegradation 31, 91–108 (2020). https://doi.org/10.1007/s10532-020-09896-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-020-09896-w