Diversity and Taxonomy of Aliphatic Hydrocarbon Producers

  • Serina L. Robinson
  • Lawrence P. Wackett
Living reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Microbially sourced alkanes and alkenes derived from fatty acids are important in nature and in society with potential as bio-based fuels and other industrial, medical, and consumer products. While the production of hydrocarbons by bacteria was first reported in the literature over half a century ago, most biosynthetic gene clusters and biochemical pathways have only been uncovered within the past decade. A deepened understanding of the genes and enzymes for fatty acid-derived hydrocarbon production has spurred genome mining efforts to determine the diversity of hydrocarbon-producing bacteria. In this chapter, we focus on prokaryotic pathways for the biosynthesis of medium- and long-chain alkanes and alkenes that have fatty acid precursors. Emphasis is placed on the taxonomy of hydrocarbon-producing organisms and the physiological and ecological role of these compounds. Hydrocarbons produced by bacteria have diverse cellular functions, including modulating membrane fluidity in response to environmental stressors. In microbial communities, hydrocarbons drive interspecies interactions and global biogeochemical cycles. Future research needs include harnessing biochemical knowledge to engineer known pathways and using genomics to better inform the discovery of novel hydrocarbon-based natural products.



We acknowledge Diego Escalante and Kelly Aukema for thoughtful comments on the manuscript. S.L.R. is supported by a NSF Graduate Research Fellowship (Grant no. 00039202).


  1. Aarts MGM, Keijzer CJ, Stiekema WJ, Pereira A (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7:2115–2127CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alata I, Jallat A, Gavilan L, Chabot M, Cruz-Diaz GA, Muñoz Caro GM, Béroff K, Dartois E (2015) Vacuum ultraviolet of hydrogenated amorphous carbons. II. Small hydrocarbons production in photon dominated regions. Astron Astrophys 584:A123CrossRefGoogle Scholar
  3. Albro PW, Dittmer JC (1969) The biochemistry of long-chain nonisoprenoid hydrocarbons. I. Characterization of the hydrocarbons of Sarcina lutea and the isolation of possible intermediates of biosynthesis. Biochemistry 8:394–405CrossRefPubMedGoogle Scholar
  4. Aukema KG, Makris TM, Stoian SA, Richman JE, Münck E, Lipscomb JD, Wackett LP (2013) Cyanobacterial aldehyde deformylase oxygenation of aldehydes yields n-1 aldehydes and alcohols in addition to alkanes. ACS Catal 3(10):2228–2238CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bailly A, Weisskopf L (2017) Mining the Volatilomes of Plant-Associated Microbiota for New Biocontrol Solutions. Front Microbiol 8Google Scholar
  6. Belcher J, McLean KJ, Matthews S, Woodward LS, Fisher K, Rigby SEJ, Nelson DR, Potts D, Baynham MT, Parker DA, Leys D, Munro AW (2014) Structure and biochemical properties of the alkene producing cytochrome P450 OleTJE (CYP152L1) from the Jeotgalicoccus sp 8456 bacterium. J Biol Chem 289:6535–6550CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beller HR, Goh EB, Keasling JD (2011) Definitive alkene identification needed for in vitro studies with ole (olefin biosynthesis) proteins. J Biol Chem 286:LE11–LE11CrossRefPubMedPubMedCentralGoogle Scholar
  8. Berla BM, Saha R, Maranas CD, Pakrasi HB (2015) Cyanobacterial alkanes modulate photosynthetic cyclic electron flow to assist growth under cold stress. Sci Rep 5:12CrossRefGoogle Scholar
  9. Bernard A, Domergue F, Pascal S, Jetter R, Renne C, Faure JD, Haslam RP, Napier JA, Lessire R, Joubes J (2012) Reconstitution of plant alkane biosynthesis in yeast demonstrates that Arabidopsis ECERIFERUM1 and ECERIFERUM3 are core components of a very-long-chain alkane synthesis complex. The Plant Cell 24(7):3106–3118Google Scholar
  10. Blom D, Fabbri C, Connor EC, Schiestl FP, Klauser DR, Boller T, Eberl L, Weisskopf L (2011) Production of plant growth modulating volatiles is widespread among rhizosphere bacteria and strongly depends on culture conditions. Environ Microbiol 13:3047–3058CrossRefPubMedGoogle Scholar
  11. Bonnett SA, Papireddy K, Higgins S, del Cardayre S, Reynolds KA (2011) Functional characterization of an NADPH dependent 2-alkyl-3-ketoalkanoic acid reductase involved in olefin biosynthesis in Stenotrophomonas maltophilia. Biochemistry 50:9633–9640CrossRefPubMedGoogle Scholar
  12. Bos LDJ, Sterk PJ, Schultz MJ (2013) Volatile metabolites of pathogens: a systematic review. PLoS Pathog 9:8CrossRefGoogle Scholar
  13. Chang ZX, Sitachitta N, Rossi JV, Roberts MA, Flatt PM, Jia JY, Sherman DH, Gerwick WH (2004) Biosynthetic pathway and gene cluster analysis of curacin A, an anti-tubulin natural product from the tropical marine cyanobacterium Lyngbya majuscula. J Nat Prod 67:1356–1367CrossRefPubMedGoogle Scholar
  14. Christenson JK, Jensen MR, Goblirsch BR, Mohamed F, Zhang W, Wilmot CM, Wackett LP (2017a) Active multienzyme assemblies for long-chain olefinic hydrocarbon biosynthesis. J Bacteriol 199:e00890-16CrossRefPubMedPubMedCentralGoogle Scholar
  15. Christenson JK, Richman JE, Jensen MR, Neufeld JY, Wilmot CM, Wackett LP (2017b) β-Lactone synthetase found in the olefin biosynthesis pathway. Biochemistry 56:348–351CrossRefPubMedPubMedCentralGoogle Scholar
  16. Christenson JK, Robinson SL, Engel TA, Richman JE, Kim AN, Wackett LP (2017c) OleB from bacterial hydrocarbon biosynthesis is a β-lactone decarboxylase that shares key features with haloalkane dehalogenases. Biochemistry 56(40):5278–5287Google Scholar
  17. Coates RC, Podell S, Korobeynikov A, Lapidus A, Pevzner P, Sherman DH, Allen EE, Gerwick L, Gerwick WH (2014) Characterization of cyanobacterial hydrocarbon composition and distribution of biosynthetic pathways. PLoS One 9:12CrossRefGoogle Scholar
  18. Damste JSS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, van Duin ACT, van Niftrik LA, Jetten MSM (2002) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419:708–712CrossRefGoogle Scholar
  19. Dermott SF, Sagan C (1995) Tidal effects of disconnected hydrocarbon seas on Titan. Nature 374(6519):238–240CrossRefPubMedGoogle Scholar
  20. Flombaum P, Gallegos JL, Gordillo RA, Rincon J, Zabala LL, Jiao NAZ, Karl DM, Li WKW, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci U S A 110:9824–9829CrossRefPubMedPubMedCentralGoogle Scholar
  21. Foo JL, Susanto AV, Keasling JD, Leong SS, Chang MW (2017) Whole-cell biocatalytic and de novo production of alkanes from free fatty acids in Saccharomyces cerevisiae. Biotechnol Bioeng 114(1):232–237CrossRefPubMedGoogle Scholar
  22. Frias JA, Richman JE, Wackett LP (2009) C-29 olefinic hydrocarbons biosynthesized by Arthrobacter species. Appl Environ Microbiol 75:1774–1777CrossRefPubMedPubMedCentralGoogle Scholar
  23. Frias JA, Richman JE, Erickson JA, Wackett LP (2011) Purification and characterization of OleA from Xanthomonas campestris and demonstration of a non-decarboxylative Claisen condensation reaction. J Biol Chem 286(13):10930–10938Google Scholar
  24. Friedman L, DaCosta B (2008) Hydrocarbon-producing genes and methods of their use. International Patent WO/2008/147781Google Scholar
  25. Gibson DT (1982) Microbial degradation of hydrocarbons. Toxicol Environ Chem 5:237–250CrossRefGoogle Scholar
  26. Goblirsch BR, Jensen MR, Mohamed F, Wackett LP, Wilmot CM (2016) Substrate trapping in crystals of the thiolase OleA identifies three channels that enable long-chain olefin biosynthesis. J Biol Chem 291:26698–26706. Scholar
  27. Grant JL, Hsieh CH, Makris TM (2015) Decarboxylation of fatty acids to terminal alkenes by cytochrome P450 compound I. J Am Chem Soc 137:4940–4943CrossRefPubMedGoogle Scholar
  28. Grant JL, Mitchell ME, Makris TM (2016) Catalytic strategy for carbon–carbon bond scission by the cytochrome P450 OleT. Proc Natl Acad Sci U S A 113:10049–10054CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gschwend P, Zafiriou OC, Gagosian RB (1980) Volatile organic compounds in seawater from the Peru upwelling region. Limnol Oceanogr 25:1044–1053CrossRefGoogle Scholar
  30. Han J, Calvin M (1969) Hydrocarbon distribution of algae and bacteria, and microbiological activity in sediments. Proc Natl Acad Sci U S A 64(2):436–443CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hopwood DA (2009) Complex enzymes in microbial natural product biosynthesis, part B: polyketides, aminocoumarins and carbohydrates. Vol. 459. Academic PressGoogle Scholar
  32. Hsieh CH, Makris TM (2016) Expanding the substrate scope and reactivity of cytochrome P450 OleT. Biochem Biophys Res Commun 476:462–466CrossRefPubMedGoogle Scholar
  33. Hunziker L, Bönisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L, Cullen D, (2015) Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl Environ Microbiol 81(3):821–830Google Scholar
  34. Jacob J (1978) Hydrocarbon and multibranched ester waxes from uropygial gland secretion of grebes. J Lipid Res 19:148–153PubMedGoogle Scholar
  35. Kancharla P, Bonnett SA, Reynolds KA (2016) Stenotrophomonas maltophilia OleC-catalyzed ATP-dependent formation of long-chain Z-olefins from 2-alkyl-3-hydroxyalkanoic acids. Chembiochem 17:1426–1429CrossRefPubMedGoogle Scholar
  36. Karlsson A, Parales JV, Parales RE, Gibson DT, Eklund H, Ramaswamy S (2003) Crystal structure of naphthalene dioxygenase: side-on binding of dioxygen to iron. Science 299:1039–1042CrossRefPubMedGoogle Scholar
  37. Katona G, Carpentier P, Niviere V, Amara P, Adam V, Ohana J, Tsanov N, Bourgeois D (2007) Raman-assisted crystallography reveals end-on peroxide intermediates in a nonheme iron enzyme. Science 316:449–453CrossRefPubMedGoogle Scholar
  38. Lea-Smith DJ, Biller SJ, Davey MP, Cotton CAR, Sepulveda BMP, Turchyn AV, Scanlan DJ, Smith AG, Chisholm SW, Howe CJ (2015) Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle. Proc Natl Acad Sci U S A 112:13591–13596CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lea-Smith DJ, Ortiz-Suarez ML, Lenn T, Nurnberg DJ, Baers LL, Davey MP, Parolini L, Huber RG, Cotton CAR, Mastroianni G, Bombelli P, Ungerer P, Stevens TJ, Smith AG, Bond PJ, Mullineaux CW, Howe CJ (2016) Hydrocarbons are essential for optimal cell size, division, and growth of cyanobacteria. Plant Physiol 172:1928–1940CrossRefPubMedPubMedCentralGoogle Scholar
  40. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nuc Acid Res 44(W1):W242–W245Google Scholar
  41. Matsunaga I, Yokotani N, Gotoh O, Kusunose E, Yamada M, Ichihara K (1997) Molecular cloning and expression of fatty acid alpha-hydroxylase from Sphingomonas paucimobilis. J Biol Chem 272:23592–23596CrossRefPubMedGoogle Scholar
  42. Matsunaga I, Ueda A, Fujiwara N, Sumimoto T, Ichihara K (1999) Characterization of the ybdT gene product of Bacillus subtilis: novel fatty acid beta-hydroxylating cytochrome P450. Lipids 34:841–846CrossRefPubMedGoogle Scholar
  43. Matthews S, Tee KL, Rattray NJ, McLean KJ, Leys D, Parker DA, Blankley RT, Munro AW (2017) Production of alkenes and novel secondary products by P450 OleT(JE) using novel H2O2-generating fusion protein systems. FEBS Lett 591:737–750CrossRefPubMedGoogle Scholar
  44. McCarthy JG, Eisman EB, Kulkarni S, Gerwick L, Gerwick WH, Wipf P, Sherman DH, Smith JL (2012) Structural basis of functional group activation by sulfotransferases in complex metabolic pathways. ACS Chem Biol 7:1994–2003CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mendez-Perez D, Begemann MB, Pfleger BF (2011) Modular synthase-encoding gene involved in alpha-olefin biosynthesis in Synechococcus sp strain PCC 7002. Appl Environ Microbiol 77:4264–4267CrossRefPubMedPubMedCentralGoogle Scholar
  46. Mendez-Perez D, Gunasekaran S, Orler VJ, Pfleger BF (2012) A translation-coupling DNA cassette for monitoring protein translation in Escherichia coli. Metab Eng 14:298–305CrossRefPubMedGoogle Scholar
  47. Mendez-Perez D, Herman NA, Pfleger BF, Nojiri H (2014) A desaturase gene involved in the formation of 1,14-nonadecadiene in Synechococcus sp. strain PCC 7002. Appl Environ Microbiol 80(19):6073–6079Google Scholar
  48. Nichols D (1995) A new n-C31:9 polyene hydrocarbon from Antarctic bacteria. FEMS Microbiol Lett 125(2–3):281–285Google Scholar
  49. Okada BK, Seyedsayamdost MR, Shen A (2017) Antibiotic dialogues: induction of silent biosynthetic gene clusters by exogenous small molecules. FEMS Microbiol Rev 41(1):19–33Google Scholar
  50. Olah GA, Molnar A (2003) Hydrocarbon chemistry. Wiley, New YorkCrossRefGoogle Scholar
  51. Pye CR (2017) Retrospective analysis of natural products provides insights for future discovery trends. Proc Natl Acad Sci U S A pii:201614680Google Scholar
  52. Qiu Y, Tittiger C, Wicker-Thomas C, Le Goff G, Young S, Wajnberg E, Fricaux T, Taquet N, Blomquist GJ, Feyereisen R (2012) An insect-specific P450 oxidative decarbonylase for cuticular hydrocarbon biosynthesis. Proc Natl Acad Sci U S A 109:14858–14863CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rajakovich LJ, Nørgaard H, Warui DM, Chang WC, Li N, Booker SJ, Krebs C, Bollinger JM Jr, Pandelia ME (2015) Rapid reduction of the diferric-peroxyhemiacetal intermediate in aldehyde-deformylating oxygenase by a cyanobacterial ferredoxin: evidence for a free-radical mechanism. J Am Chem Soc 137(36):11695–11709CrossRefPubMedGoogle Scholar
  54. Romero D, Traxler MF, Lopez D, Kolter R (2011) Antibiotics as signal molecules. Chem Rev 111:5492–5505CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rude MA, Baron TS, Brubaker S, Alibhai M, Del Cardayre SB, Schirmer A (2011) Terminal olefin (1-alkene) biosynthesis by a novel P450 fatty acid decarboxylase from Jeotgalicoccus species. Appl Environ Microbiol 77:1718–1727CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rui Z, Li X, Zhu XJ, Liu J, Domigan B, Barr I, Cate JHD, Zhang WJ (2014) Microbial biosynthesis of medium-chain 1-alkenes by a nonheme iron oxidase. Proc Natl Acad Sci U S A 111:18237–18242CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rui Z, Harris NC, Zhu XJ, Huang W, Zhang WJ (2015) Discovery of a family of desaturase-like enzymes for 1-alkene biosynthesis. ACS Catal 5:7091–7094CrossRefGoogle Scholar
  58. Schirmer A, Rude MA, Li XZ, Popova E, del Cardayre SB (2010) Microbial biosynthesis of alkanes. Science 329:559–562CrossRefPubMedGoogle Scholar
  59. Schmidt R, Etalo DW, de Jager V, Gerards S, Zweers H, de Boer W, Garbeva P (2016) Microbial small talk: volatiles in fungal–bacterial interactions. Front Microbiol 6:1495Google Scholar
  60. Schwarzenbach RP, Bromund RH, Gschwend PM, Zafiriou OC (1978) Volatile organic compounds in coastal seawater. Org Geochem 1:93–107CrossRefGoogle Scholar
  61. Seyedsayamdost MR (2014) High-throughput platform for the discovery of elicitors of silent bacterial gene clusters. Proc Natl Acad Sci USA 111(20):7266–7271Google Scholar
  62. Shaw JJ, Spakowicz DJ, Dalal RS, Davis JH, Lehr NA, Dunican BF, Orellana EA, Narvaez-Trujillo A, Strobel SA (2015) Biosynthesis and genomic analysis of medium-chain hydrocarbon production by the endophytic fungal isolate Nigrograna mackinnonii E5202H. Appl Microbiol Biotechnol 99:3715–3728CrossRefPubMedPubMedCentralGoogle Scholar
  63. Shokri A, Que L Jr (2015) Conversion of aldehyde to alkane by a peroxoiron(III) oxygenase. J Am Chem Soc 137(24):7686–7691CrossRefPubMedPubMedCentralGoogle Scholar
  64. Snow TP, McCall BJ (2006) Diffuse atomic and molecular clouds. Ann Rev Astron Astrophys 44:367–414CrossRefGoogle Scholar
  65. Stephenson M, Stickland LH (1933) The bacterial formation of methane by the reduction of one-carbon compounds by molecular hydrogen. Biochem J 27:1517–1527CrossRefPubMedPubMedCentralGoogle Scholar
  66. Strobel GA, Knighton B, Kluck K, Ren YH, Livinghouse T, Griffin M, Spakowicz D, Sears J (2008) The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum (NRRL 50072). Microbiology 154:3319–3328CrossRefPubMedGoogle Scholar
  67. Sukovich DJ, Seffernick JL, Richman JE, Gralnick JA, Wackett LP (2010a) Widespread head-to-head hydrocarbon biosynthesis in bacteria and role of OleA. Appl Environ Microbiol 76:3850–3862CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sukovich DJ, Seffernick JL, Richman JE, Hunt KA, Gralnick JA, Wackett LP (2010b) Structure, function, and insights into the biosynthesis of a head-to-head hydrocarbon in Shewanella oneidensis strain MR-1. Appl Environ Microbiol 76:3842–3849CrossRefPubMedPubMedCentralGoogle Scholar
  69. Thomas JB (1950) On the role of the carotenoids in photosynthesis in Rhodospirillum rubrum. Biochim Biophys Acta 5(2):186–196PubMedGoogle Scholar
  70. Tornabene TG, Bennett EO, Oró J (1967) Fatty acid and aliphatic hydrocarbon composition of Sarcina lutea grown in three different media. J Bacteriol 94(2):344–348PubMedPubMedCentralGoogle Scholar
  71. U.S. Energy Information Administration (2017) International energy statistics. Available at
  72. Verdier-Pinard P, Lai JY, Yoo HD, Yu JR, Marquez B, Nagle DG, Nambu M, White JD, Falck JR, Gerwick WH, Day BW, Hamel E (1998) Structure-activity analysis of the interaction of curacin A, the potent colchicine site antimitotic agent, with tubulin and effects of analogs on the growth of MCF-7 breast cancer cells. Mol Pharmacol 53:62–76CrossRefPubMedGoogle Scholar
  73. Whicher JR, Smaga SS, Hansen DA, Brown WC, Gerwick WH, Sherman DH, Smith JL (2013) Cyanobacterial polyketide synthase docking domains: a tool for engineering natural product biosynthesis. Chem Biol 20:1340–1351CrossRefPubMedGoogle Scholar
  74. Whicher JR, Dutta S, Hansen DA, Hale WA, Chemler JA, Dosey AM, Narayan ARH, Hakansson K, Sherman DH, Smith JL, Skiniotis G (2014) Structural rearrangements of a polyketide synthase module during its catalytic cycle. Nature 510:560CrossRefPubMedPubMedCentralGoogle Scholar
  75. Winters K, Parker PL, Van Baalen C (1969) Hydrocarbons of blue-green algae: geochemical significance. Science 163:467–468CrossRefPubMedGoogle Scholar
  76. Yoon JH, Lee KC, Weiss N, Kang KH, Park YH (2003) Jeotgalicoccus halotolerans gen nov, sp nov and Jeotgalicoccus psychrophilus sp nov, isolated from the traditional Korean fermented seafood jeotgal. Int J Syst Evol Microbiol 53:595–602CrossRefPubMedGoogle Scholar
  77. Zhang L, Hashimoto T, Qin B, Hashimoto J, Kozone I, Kawahara T, Okada M, Awakawa T, Ito T, Asakawa Y, and Ueki M (2017) Characterization of giant modular PKSs provides insight into genetic mechanism for structural diversification of aminopolyol polyketides. Ang Chem Int Ed, 56(7), pp. 1740–1745Google Scholar
  78. Zobell CE (1946) Action of microörganisms on hydrocarbons. Bacteriol Rev 10(1):1–49PubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  1. 1.Department of Microbiology and ImmunologyUniversity of Minnesota, Twin CitiesSt. PaulUSA
  2. 2.BioTechnology InstituteUniversity of Minnesota, Twin CitiesSt. PaulUSA
  3. 3.Department of Biochemistry, Molecular Biology and BiophysicsUniversity of Minnesota, Twin CitiesSt. PaulUSA

Personalised recommendations