Abstract
Petroleum (or crude oil) is a complex mixture of hydrocarbons. Annually, millions of tons of crude petroleum oil enter the marine environment from either natural or anthropogenic sources. Hydrocarbon-degrading bacteria (HDB) are able to assimilate and metabolize hydrocarbons present in petroleum. Crude oil pollution constitutes a temporary condition of carbon excess coupled to a limited availability of nitrogen that prompts marine oil-degrading bacteria to accumulate storage compounds. Storage lipid compounds such as polyhydroxyalkanoates (PHAs), triacylglycerols (TAGs), or wax esters (WEs) constitute the main accumulated lipophilic substances by bacteria under such unbalanced growth conditions. The importance of these compounds as end-products or precursors to produce interesting biotechnologically relevant chemicals has already been recognized. In this review, we analyze the occurrence and accumulation of lipid storage in marine hydrocarbonoclastic bacteria. We further discuss briefly the production and export of lipophilic compounds by bacteria belonging to the Alcanivorax genus, which became a model strain of an unusual group of obligate hydrocarbonoclastic bacteria (OHCB) and discuss the possibility to produce neutral lipids using A. borkumensis SK2.
Similar content being viewed by others
References
Abraham W-R, Meyer H, Yakimov M (1998) Novel glycine containing glucolipids from the alkane using bacterium Alcanivorax borkumensis. Biochim Biophys Acta 1393:57–62
Alvarez HM, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367–376
Alvarez HM, Mayer F, Fabritius D, Steinbüchel A (1996) Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol 165:377–386
Alvarez HM, Pucci OH, Steinbüchel A (1997a) Lipid storage compounds in marine bacteria. Appl Microbiol Biotechnol 47:132–139
Alvarez HM, Kalscheuer R, Steinbüchel A (1997b) Accumulation of storage lipids in species of Rhodococcus and Nocardia and effects of inhibitors and polyethylene glycol. Fett/Lipid 99:239–246
Alvarez HM, Luftmann H, Silva RA, Cesari AC, Viale A, Wältermann M, Steinbüchel A (2002) Identification of phenyldecanoic acid as a constituent of triacylglycerols and wax ester produced by Rhodococcus opacus PD630. Microbiology (SGM) 148:1407–1412
Anderson A, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54:450–472
Atlas RM (1981) Microbial degradation of petroleum hydrocarbons: an environmental perspective. Microbiol Rev 45:180–209
Atlas RM (1995) Petroleum biodegradation and oil spill bioremediation. Mar Pollut Bull 31:178–182
Bacchin P, Robertiello A, Viglia A (1974) Identification of n-decane oxidation products in Corynebacterium cultures by combined gas chromatography-mass spectrometry. Appl Microbiol 28:737–741
Bergé JP, Barnathan G (2005) Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Adv Biochem Eng Biotechnol 96:49–125
Bogan BW, Sullivan WR, Kayser KJ, Derr KD, Aldrich HC, Paterek R (2003) Alkanindiges illinoisensis gen. nov., sp. nov., an obligately hydrocarbonoclastic, aerobic squalane-degrading bacterium isolated from oilfield soils. Int J Syst Evol Microbiol 53:1389–1395
Bredemeier R, Hulsch R, Metzger JO, Berthe-Corti L (2003) Submersed culture production of extracellular wax esters by the marine bacterium Fundibacter jadensis. Mar Biotechnol 5:579–583
Bruns A, Berthe-Corti L (1999) Fundibacter jadensis gen. nov., sp. nov., a new slightly halophilic bacterium, isolated from intertidal sediment. Int J Sys Bacteriol 49:441–448
Bryn K, Jantzen E, Bovre K (1977) Occurrence and patterns of waxes in Neisseriaceae. J Gen Microbiol 102:33–43
Capello S, Denaro R, Genovese M, Giuliano L, Yakimov MM (2007) Predominant growth of Alcanivorax during experiments on “oil spill bioremediation” in mesocosms. Microbiol Res 162:185–190
Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64
Dyksterhouse SE, Gray JP, Herwig RP, Lara JC, Staley JT (1995) Cycloclasticus pugetii gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium from marine sediments. Int J Syst Bacteriol 45:116–123
Fernández-Martínez J, Pujalte MJ, García-Martínez J, Mata M, Garay E, Rodríguez-Varela F (2003) Description of Alcanivorax venustensis sp. nov. and reclassification of Fundibacter jadensis DSM12178T (Bruns and Berthe-Corti 1999) as Alcanivorax jadensis comb. nov., members of the emended genus Alcanivorax. Int J Syst Evol Microbiol 53:331–338
Fixter LM, Fewson CA (1974) The accumulation of waxes by Acinetobacter calcoaceticus NCIB-8250. Biochem Soc Trans 2:944–945
Fixter LM, Nagi MN, McCormack JG, Fewson CA (1986) Structure, distribution and function of wax esters in Acinetobacter calcoaceticus. J Gen Microbiol 132:3147–3157
Fulco AJ (1983) Fatty acid metabolism in bacteria. Prog Lipid Res 22:133–160
Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P, Bertrand JC (1992) Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 42:568–576
Gertler C, Gerdts G, Timmis KN, Yakimov MM, Golyshin PN (2009a) Populations of heavy fuel oil-degrading marine microbial community in presence of oil sorbent materials. J Appl Microbiol 107:590–605
Gertler C, Gerdts G, Timmis KN, Golyshin PN (2009b) Microbial consortia in mesocosm bioremediation trial using oil sorbents, slow-release fertilizer and bioaugmentation. FEMS Microbiol Ecol 69:288–300
Golyshin PN, Chernikova T, Abraham WR, Lünsdorf H, Timmis KN, Yakimov MM (2002) Oleiphilaceae fam. nov., to include Oleiphilus messinensis gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 52:901–911
Goutx M, Acquaviva M, Bertrand JC (1990) Cellular and extracellular carbohydrates and lipids from marine bacteria during growth on soluble substrates and hydrocarbons. Mar Ecol Prog Ser 61:291–296
Haferburg D, Hommel R, Claus R, Kleber HP (1986) Extracellular microbial lipids as biosurfactants. Adv Biochem Eng Biotechnol 33:53–93
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
Harayama S, Kishira H, Kasai Y, Shutsubo K (1999) Petroleum biodegradation in marine environments. J Mol Microbiol Biotechnol 1:63–70
Head IM (1998) Bioremediation: towards a credible technology. Microbiology (SGM) 144:599–608
Head IM, Swanell RPJ (1999) Bioremediation of petroleum hydrocarbon contaminants in marine habitats. Curr Opin Biotechnol 10:234–239
Head IM, Jones DM, Röling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182
Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT (1999) Polyciclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov. Appl Environ Microbiol 65:251–259
Holtzapple E, Schmidt-Dannert C (2007) Biosynthesis of isoprenoid wax ester in Marinobacter hydrocarbonoclasticus DSM 8798: Identification and characterization of isoprenoid coenzyme A synthetase and wax ester synthases. J Bacteriol 189:3804–3812
Hommel RK (1990) Formation and physiological role of biosurfactants produced by hydrocarbon-utilizing microorganisms. Biodegradation 1:107–119
Ishige T, Tani A, Sakai Y, Kato N (2003) Wax ester production by bacteria. Curr Opin Microbiol 6:244–250
Kalscheuer R, Steinbüchel A (2003) A novel bifunctional wax ester synthase/acyl-CoA:diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J Biol Chem 278:8075–8082
Kalscheuer R, Wältermann M, Alvarez HM, Steinbüchel A (2001) Preparative isolation of lipid inclusions from Rhodococcus opacus and Rhodococcus ruber and identification of granule-associated proteins. Arch Microbiol 177:20–28
Kalscheuer R, Stöveken T, Malkus U, Reichelt R, Golyshin PN, Sabirova JS, Ferrer M, Timmis KN, Steinbüchel A (2007) Analysis of storage lipid accumulation in Alcanivorax borkumensis: evidence for alternative triacylglycerol biosynthesis routes in bacteria. J Bacteriol 189:918–928
Kasai Y, Kishira H, Sasaki T, Syutsubo K, Watanabe K, Harayama S (2002a) Predominant growth of Alcanivorax strains in oil-contaminated and nutrient-supplemented sea water. Environ Microbiol 4:141–147
Kasai Y, Kishira H, Harayama S (2002b) Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol 68:5625–5633
Klein B, Grossi V, Bouriat P, Goulas P, Grimaud R (2008) Cytoplasmic wax ester accumulation during biofilm-driven substrate assimilation at the alkane-water interface by Marinobacter hydrocarbonoclasticus SP17. Res Microbiol 159:137–144
Lageveen RG, Huisman GW, Preusting H, Ketelaar P, Eggink G, Witholt B (1988) Formation of polyesters by Pseudomonas oleovorans: Effect of substrates on formation and composition of poly-(R)-3-hydroxyalkanoates and poly-(R)-3-hydroxyalkenoates. Appl Environ Microbiol 54:2924–2932
Lemoigne M (1926) Produits de déshydration et de polymerisation de l’acide b-oxobutyrique. Bull Soc Chem Biol (Paris) 8:770–782
Lenz RW, Marchessault RH (2005) Bacterial polyesters: biosynthesis, biodegradable plastics and biotechnology. Biomacromolecules 6:1–8
Li Q, Du W, Liu D (2008) Perspectives of microbial oils for biodiesel production. Appl Microbiol Biotechnol 80:749–756
Liu C, Shao Z (2005) Alcanivorax dieselolei sp. nov., a novel alkane-degrading bacterium isolated from sea water and deep-sea sediment. Int J Syst Evol Microbiol 55:1181–1186
Makula RA, Lockwood PJ, Finnerty WR (1975) Comparative analysis of the lipids of Acinetobacter species grown on hexadecane. J Bacteriol 121:250–258
Maneerat S (2005) Biosurfactants from marine microorganisms. Songklanakarin J Sci Technol 27:1263–1272
Manilla-Pérez E, Reers C, Baumgart M, Hetzler S, Reichelt R, Malkus U, Kalscheuer R, Wältermann M, Steinbüchel A (2010) Analysis of lipid export in hydrocarbonoclastic bacteria of the genus Alcanivorax: identification of lipid export-negative mutants of A. borkumensis SK2 and A. jadensis T9. J Bacteriol 192:643–656
Maruyama A, Ishiwata H, Kitamura K, Sunamura M, Fujita T, Matsuo M, Higashihara T (2003) Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill. Microb Ecol 46:442–453
Mashburn-Warren LM, Whiteley M (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846
McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007a) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176
McKew BA, Coulon F, Yakimov MM, Denaro R, Genovese M, Smith CJ, Osborn AM, Timmis KN, McGenity TJ (2007b) Efficacy of intervention strategies for bioremediation of crude oil in marine systems and effects on indigenous hydrocarbonoclastic bacteria. Environ Microbiol 9:1562–1571
Mukherjee S, Das P, Sen R (2006) Towards commercial production of microbial surfactants. Trends Biotechnol 24:509–515
Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VAP, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen J, Timmis KN, Düsterhöft A, Tümmler B, Fraser CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4:799–808
Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with surfaces. Microbiol Rev 60:151–166
Olukoshi ER, Packter NM (1994) Importance of stored triacylglycerols in Streptomyces: possible carbon source for antibiotics. Microbiology (SGM) 140:931–943
Paulsen IT, Park JH, Choi SP, Saier MH Jr (1997) A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol Rev 156:1–8
Prieto MA (2007) From oil to bioplastics, a dream come true? J Bacteriol 189:289–290
Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183:27–36
Raymond RL, Davis JB (1960) n-alkane utilization and lipid formation by a Nocardia. Appl Microbiol 8:329–334
Rehm BHA (2003) Polyester synthases: natural catalysts for plastics. Biochem J 376:15–33
Rivas R, García-Fraile P, Peix A, Mateos PF, Martínez-Molina E, Velázquez E (2007) Alcanivorax balearicus sp. nov., isolated from Lake Martel. Int J Syst Evol Microbiol 57:1331–1335
Röling WF, Milner MG, Jones DM, Lee K, Daniel F, Swanell RJ, Head IM (2002) Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil-spill bioremediation. Appl Environ Microbiol 68:5537–5548
Röling WF, Milner MG, Jones DM, Fratepietro F, Swanell RJ, Daniel F, Head IM (2004) Bacterial community dynamics and hydrocarbon degradation during a field-scale evaluation of bioremediation on a mudflat beach contaminated with buried oil. Appl Environ Microbiol 70:2603–2613
Ron EZ, Rosenberg E (2002) Biosurfactants and oil bioremediation. Curr Opin Biotechnol 13:249–252
Rontani JF, Bonin PC, Volkman JK (1999) Production of wax esters during aerobic growth of marine bacteria on isoprenoid compounds. Appl Environ Microbiol 65:221–230
Rosenberg M, Rosenberg E (1985) Bacterial adherence at the hydrocarbon–water interface. Oil Petrochem Pollut 2:155–162
Rosenberg E, Ron EZ (1999) High- and low-molecular-mass microbial surfactants. Appl Microbiol Biotechnol 52:154–162
Rosenberg E, Legmann R, Kushmaro A, Taube R, Adler E, Ron E (1992) Petroleum bioremediation: a multiphase problem. Biodegradation 3:337–350
Russel NJ, Volkman JK (1980) The effect of growth temperature and wax ester composition in the psychrophilic bacterium Micrococcus cryophilus ATCC 15174. J Gen Microbiol 118:131–141
Sabirova JS, Ferrer M, Lünsdorf H, Wray V, Kalscheuer R, Steinbüchel A, Timmis KN, Golyshin PN (2006) Mutation in a “tesB-like” hydroxyacil-coenzyme A-specific thioesterase gene causes hyperproduction of extracellular polyhydoxyalkanoates by Alcanivorax borkumensis SK2. J Bacteriol 188:8452–8459
Sabirova JS, Chernikova TN, Timmis KN, Golyshin PN (2008) Niche-specificity factors of a marine oil-degrading bacterium Alcanivorax borkumensis SK2. FEMS Microbiol Lett 285:89–96
Samiullah Y (1985) Biological effects of marine oil pollution. Oil Petrochem Pollut 2:235–264
Schneiker S, Martins dos Santos VAP, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T, Pühler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Vorhölter FJ, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24:997–1004
Schörken U, Kempers P (2009) Lipid biotechnology: industrially relevant production processes. Eur J Lipid Sci Technol 111:627–645
Scott CCL, Finnerty WR (1976) Characterization of intracytoplasmic hydrocarbon inclusions from hydrocarbon-oxidizing Acinetobacter species HO1-N. J Bacteriol 127:481–489
Singer ME, Tyler SM, Finnerty WR (1985) Growth of Acinetobacter sp. strain HO1-N on n-hexadecanol: physiological and ultrastructural characteristics. J Bacteriol 162:162–169
Singh A, van Hamme JD, Ward OP (2007) Surfactants in microbiology and biotechnology: part 2. Application aspects. Biotechnol Adv 25:99–121
Steinbüchel A (2001) Perspectives for biotechnological production and utilization of biopolymers: metabolic engineering of polyhydroxyalkanoate biosynthesis pathways as a successful example. Macromol Biosci 1:1–24
Steinbüchel A, Valentin HE (1995) Diversity of bacterial polyhydroxyalkanoic acids. FEMS Microbiol Lett 128:219–228
Stephanopoulos GN, Aristidou AA, Nielsen J (1998) Metabolic engineering: principles and methodologies. Academic, USA
Syutsubo K, Kishira H, Harayama S (2001) Development of specific oligonucleotide probes for the identification and in situ detection of hydrocarbon-degrading Alcanivorax strains. Environ Microbiol 3:371–379
Timm A, Steinbüchel A (1990) Formation of polyesters consisting of medium-chain-length 3-hydroxyalkanoic acids from gluconate by Pseudomonas aeruginosa and other fluorescent pseudomonads. Appl Environ Microbiol 56:3360–3367
van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21
van Beilen JB, Li Z, Duetz WA, Smits THM, Witholt B (2003) Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci Technol Rev IFP 58:427–440
van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549
van Hamme JD, Singh A, Ward OP (2006) Physiological aspects. Part1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnol Adv 24:604–620
Wältermann M, Steinbüchel A (2005) Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J Bacteriol 187:3607–3619
Wältermann M, Steinbüchel A (2006) Wax ester and triacylglycerols inclusions. In: Shively JM, Steinbüchel A (eds) Inclusions in prokaryotes (Microbiology Monographs, vol. 1). Springer, Heidelberg, pp 137–166
Wang L, Schnoes HK, Takayama K, Goldman DS (1972) Synthesis of alcohol and wax ester by a cell-free system in Mycobacterium tuberculosis. Biochem Biophys Acta 260:41–48
Wentzel A, Ellingsen TE, Kotlar HK, Zotchev SB, Throne-Holst M (2007) Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol 76:1209–1221
Wu Y, Lai Q, Zhou Z, Qiao N, Liu C, Shao Z (2009) Alcanivorax hongdengensis sp. nov., an alkane-degrading bacterium isolated from surface seawater of the straits of Malacca and Singapore, producing a lipopeptide as its biosurfactant. Int J Syst Evol Microbiol 59:1474–1479
Yakimov MM, Golyshin PN, Lang S, Moore ERB, Abraham WR, Lünsdorf H, Timmis KN (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 48:339–348
Yakimov MM, Giuliano L, Gentile G, Crisafi E, Chernikova TN, Abraham WR, Lünsdorf H, Timmis KN, Golyshin PN (2003) Oleispira antarctica gen. nov., sp. nov., a novel hydrocarbonoclastic marine bacterium isolated from Antarctic coastal sea water. Int J Syst Evol Microbiol 53:779–785
Yakimov MM, Giuliano L, Denaro R, Crisafi E, Chernikova TN, Abraham WR, Lünsdorf H, Timmis KN, Golyshin PN (2004) Thalassolituus oleivorans gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 54:141–148
Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, Timmis KN, Golyshin PN, Giuliano L (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7:1426–1441
Yakimov MM, Timmis KN, Golyshin P (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266
ZoBell CE (1946) Action of microorganisms on hydrocarbons. Bacteriol Rev 10:1–49
Acknowledgments
Financial support by the Deutsche Forschungsgemeinschaft (DFG) to AS (STE.386/76-3) is much acknowledged. E. Manilla-Pérez is indebted to the Deutscher Akademischer Austauschdienst (DAAD, Germany) and the National Council on Science and Technology (CONACyT, México) for the award of doctoral scholarship.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Manilla-Pérez, E., Lange, A.B., Hetzler, S. et al. Occurrence, production, and export of lipophilic compounds by hydrocarbonoclastic marine bacteria and their potential use to produce bulk chemicals from hydrocarbons. Appl Microbiol Biotechnol 86, 1693–1706 (2010). https://doi.org/10.1007/s00253-010-2515-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-010-2515-5