Skip to main content

Advertisement

Log in

Polyunsaturated fatty acids in marine bacteria and strategies to enhance their production

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Polyunsaturated fatty acids (PUFAs) play an important role in human diet. Despite the wide-ranging importance and benefits from heart health to brain functions, humans and mammals cannot synthesize PUFAs de novo. The primary sources of PUFA are fish and plants. Due to the increasing concerns associated with food security as well as issues of environmental contaminants in fish oil, there has been considerable interest in the production of polyunsaturated fatty acids from alternative resources which are more sustainable, safer, and economical. For instance, marine bacteria, particularly the genus of Shewanella, Photobacterium, Colwellia, Moritella, Psychromonas, Vibrio, and Alteromonas, are found to be one among the major microbial producers of polyunsaturated fatty acids. Recent developments in the area with a focus on the production of polyunsaturated fatty acids from marine bacteria as well as the metabolic engineering strategies for the improvement of PUFA production are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abd Elrazak A, Ward AC, Glassey J (2013) Polyunsaturated fatty acid production by marine bacteria. Bioprocess Biosyst Eng 36:1641–1652

    Article  PubMed  CAS  Google Scholar 

  • Alain K, Marteinsson VT, Miroshnichenko ML, Bonch-Osmolovskaya EA, Prieur D, Birrien J-L (2002) Marinitoga piezophila sp. nov., a rod-shaped, thermo-piezophilic bacterium isolated under high hydrostatic pressure from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 52:1331–1339

    PubMed  CAS  Google Scholar 

  • Allen EE, Bartlett DH (2002) Structure and regulation of the omega-3 polyunsaturated fatty acid synthase genes from the deep-sea bacterium Photobacterium profundum strain SS9. Microbiology 148:1903–1913

    Article  PubMed  CAS  Google Scholar 

  • Allen EE, Facciotti D, Bartlett DH (1999) Monounsaturated but not polyunsaturated fatty acids are required for growth of the deep-sea bacterium Photobacterium profundum SS9 at high pressure and low temperature. Appl Environ Microbiol 65:1710–1720

    PubMed  PubMed Central  CAS  Google Scholar 

  • Amiri-Jami M, Abdelhamid AG, Hazaa M, Kakuda Y, Griffths MW (2015) Recombinant production of omega-3 fatty acids by probiotic Escherichia coli Nissle 1917. FEMS Microbiol Lett 362:20

    Article  Google Scholar 

  • Amiri-Jami M, LaPointe G, Griffiths MW (2014) Engineering of EPA/DHA omega-3 fatty acid production by Lactococcus lactis subsp. cremoris MG1363. Appl Microbiol Biotechnol 98:3071–3080

    Article  PubMed  CAS  Google Scholar 

  • Amiri-Jami M, Wang H, Kakuda Y, Griffiths MW (2006) Enhancement of polyunsaturated fatty acid production by Tn5 transposon in Shewanella baltica. Biotechnol Lett 28:1187–1192

    Article  PubMed  CAS  Google Scholar 

  • Amiri-Jami M, Griffiths M (2010) Recombinant production of omega-3 fatty acids in Escherichia coli using a gene cluster isolated from Shewanella baltica MAC1. J App Microbiol 109:1897–1905

    Article  CAS  Google Scholar 

  • Auman AJ, Breezee JL, Gosink JJ, Schumann P, Barnes CR, Kampfer P, Staley JT (2010) Psychromonas boydii sp. nov., a gas-vacuolate, psychrophilic bacterium isolated from an Arctic sea-ice core. Int J Syst Evol Microbiol 60:84–92

    Article  PubMed  CAS  Google Scholar 

  • Baumann L, Baumann P, Mandel M, Allen RD (1972) Taxonomy of aerobic marine eubacteria. J Bacteriol 110:402–429

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bays HE, Ballantyne CM, Kastelein JJ, Isaacsohn JL, Braeckman RA, Soni PN (2011) Eicosapentaenoic acid ethyl ester (AMR101) therapy in patients with very high triglyceride levels (from the multi-center, placebo-controlled, randomized, double-blind, 12-week study with an open-label extension [MARINE] trial). Am J Cardiol 108:682–690

    Article  PubMed  CAS  Google Scholar 

  • Bazan NG (2009) Neuroprotectin D1-mediated anti-inflammatory and survival signaling in stroke, retinal degenerations, and Alzheimer’s disease. J Lipid Res 50:400–405

    Article  CAS  Google Scholar 

  • Benediktsdottir E, Verdonck L, Sproer C, Helgason S, Swings J (2000) Characterization of Vibrio viscosus and Vibrio wodanis isolated at different geographical locations: a proposal for reclassification of Vibrio viscosus as Moritella viscosa comb. nov. Int J Syst Evol Microbiol 50:479–488

    Article  PubMed  CAS  Google Scholar 

  • Bergé J-P, Barnathan G (2005) Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Springer, Berlin, pp 49–125

    Google Scholar 

  • Bianchi AC, Olazábal L, Torre A, Loperena L (2014) Antarctic microorganisms as source of the omega-3 polyunsaturated fatty acids. World J Microbiol Biotechnol 30:1869–1878

    Article  PubMed  CAS  Google Scholar 

  • Bowman JP, Gosink JJ, Mccammon SA, Lewis TE, Nichols DS, Nichols PD, Skerratt JH, Staley JT, Mcmeekin TA (1998) Colwellia demingiae sp. nov., Colwellia hornerae sp. nov., Colwellia rossensis sp. nov. and Colwellia psychrotropica sp. nov.: psychrophilic Antarctic species with the ability to synthesize docosahexaenoic acid (22:63). Int J Syst Bacteriol 48:1171–1180

    Article  CAS  Google Scholar 

  • Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997a) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bowman JP, McCammon SA, Nichols DS, Skerratt JH, Rea SM, Nichols PD, McMeekin TA (1997b) Shewanella gelidimarina sp. nov. and Shewanella frigidimarina sp. nov., novel antarctic species with the ability to produce eicosapentaenoic acid (20:5 3) and grow anaerobically by dissimilatory Fe(III) reduction. Int J Syst Bacteriol 47:1040–1047

    Article  PubMed  CAS  Google Scholar 

  • Cao Y, Cao Y, Zhao M (2012) Biotechnological production of eicosapentaenoic acid: from a metabolic engineering point of view. Process Biochem 47:1320–1326

    Article  CAS  Google Scholar 

  • Cao Y, Chastain RA, Eloe EA, Nogi Y, Kato C, Bartlett DH (2014) Novel psychropiezophilic Oceanospirillales species Profundimonas piezophila gen. nov., sp. nov., isolated from the deep-sea environment of the Puerto Rico Trench. Appl Environ Microbiol 80:54–60

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Das UN, Fams (2003) Long-chain polyunsaturated fatty acids in the growth and development of the brain and memory. Nutrition 19:62–65

    Article  PubMed  CAS  Google Scholar 

  • Davis MS, Solbiati J, Cronan JE (2000) Overproduction of acetyl-CoA carboxylase activity increases the rate of fatty acid biosynthesis in Escherichia coli. J Biol Chem 275:28593–28598

    Article  PubMed  CAS  Google Scholar 

  • de Carvalho CCCR, Caramujo MJ (2012) Lipids of prokaryotic origin at the base of marine food webs. Mar Drugs 10:2698–2714

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de Carvalho CCCR, Fernandes P (2010) Production of metabolites as bacterial responses to the marine environment. Mar Drugs 8:705–727

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Delong EF, Franks DG, Yayanos AA (1997) Evolutionary relationships of cultivated psychrophilic and barophilic deep-sea bacteria. Appl Environ Microbiol 63:2105–2108

    PubMed  PubMed Central  CAS  Google Scholar 

  • Delong EF, Yayanos AA (1987) Properties of the glucose transport system in some deep-sea bacteria. Appl Environ Microbiol 53:527–532

    PubMed  PubMed Central  CAS  Google Scholar 

  • Delong EF, Yayanos AA (1986) Biochemical function and ecological significance of novel bacterial lipids in deep-sea procaryotes. Appl Environ Microbiol 51:730–737

    PubMed  PubMed Central  CAS  Google Scholar 

  • Deming JW, Hada H, Colwell RR, Luehrsen KR, Fox GE (1984) The ribonucleotide sequence of 5S rRNA from two strains of deep-sea barophilic bacteria. Microbiol 130:1911–1920

    Article  CAS  Google Scholar 

  • Deming JW, Somers LK, Straube WL, Swartz DG, Macdonell MT (1988) Isolation of an Obligately Barophilic Bacterium and Description of a New Genus, Colwellia gen. nov.. Syst Appl Microbiol 10(2):152–160

    Article  Google Scholar 

  • Domingo JL, Bocio A, Falcó G, Llobet JM (2007) Benefits and risks of fish consumption. Part I. A quantitative analysis of the intake of omega-3 fatty acids and chemical contaminants. Toxicology 230:219–226

    Article  PubMed  CAS  Google Scholar 

  • Fang J, Barcelona MJ, Abrajano T, Nogi Y, Kato C (2002) Isotopic composition of fatty acids of extremely piezophilic bacteria from the Mariana Trench at 11,000 m. Mar Chem 80:1–9

    Article  CAS  Google Scholar 

  • Fang J, Barcelona MJ, Nogi Y, Kato C (2000) Biochemical implications and geochemical significance of novel phospholipids of the extremely barophilic bacteria from the Marianas Trench at 11,000 m. Deep Sea Res I Oceanogr Res Pap 47:1173–1182

    Article  CAS  Google Scholar 

  • Fang J, Kato C (2007) FAS or PKS, lipid biosynthesis and stable carbon isotope fractionation in deep-sea piezophilic bacteria. Commun Curr Res Educ Top Trends Appl Microbiol 1:190–200

    Google Scholar 

  • Fang J, Kato C, Sato T, Chan O, McKay D (2004) Biosynthesis and dietary uptake of polyunsaturated fatty acids by piezophilic bacteria. Comp Biochem Physiol B Biochem Mol Biol 137:455–461

    Article  PubMed  CAS  Google Scholar 

  • Freese E, Rütters H, Köster J, Rullkötter J, Sass H (2009) Gammaproteobacteria as a possible source of eicosapentaenoic acid in anoxic intertidal sediments. Microb Ecol 57:444–454

    Article  PubMed  CAS  Google Scholar 

  • Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875

    Article  PubMed  CAS  Google Scholar 

  • Gauthier G, Gauthier M, Christen R (1995) Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int J Syst Bacteriol 45:755–761

    Article  PubMed  CAS  Google Scholar 

  • Gemperlein K, Zipf G, Bernauer HS, Müller R, Wenzel SC (2016) Metabolic engineering of Pseudomonas putida for production of docosahexaenoic acid based on a myxobacterial PUFA synthase. Metab Eng 33:98–108

    Article  PubMed  CAS  Google Scholar 

  • Gladyshev MI, Sushchik NN, Makhutova ON (2013) Production of EPA and DHA in aquatic ecosystems and their transfer to the land. Prostaglandins Other Lipid Mediat 107:117–126

    Article  PubMed  CAS  Google Scholar 

  • Gong Y, Wan X, Jiang M, Hu C, Hu H, Huang F (2014) Metabolic engineering of microorganisms to produce omega-3 very long-chain polyunsaturated fatty acids. Prog Lipid Res 56:19–35

    Article  PubMed  CAS  Google Scholar 

  • Hamamoto T, Takata N, Kudo T, Horikoshi K (1995) Characteristic presence of polyunsaturated fatty acids in marine psychrophilic vibrios. FEMS Microbiol Lett 129:51–56

    Article  CAS  Google Scholar 

  • Hamamoto T, Takata N, Kudo T, Horikoshi K (1994) Effect of temperature and growth phase on fatty acid composition of the psychrophilic Vibrio sp. strain no. 5710. FEMS Microbiol Lett 119:77–81

    Article  CAS  Google Scholar 

  • Hayashi S, Satoh Y, Ujihara T, Takata Y, Dairi T (2016) Enhanced production of polyunsaturated fatty acids by enzyme engineering of tandem acyl carrier proteins. Sci Rep 6:35441

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hong S-Y, Seip J, Sharpe PL, Xue Z, Yadav NS, Zhang H ZQ (2011) Recombinant microbial host cells for high eicosapentaenoic acid production. U.S. Patent Application 20120052537

  • Hori R, Nishida T, Okuyama H (2011) Hydrophilic and hydrophobic compounds antithetically affect the growth of eicosapentaenoic acid-synthesizing Escherichia coli recombinants. Open Microbiol J 5:114–118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hosoya S, Jang J-H, Yasumoto-Hirose M, Matsuda S, Kasai H (2009) Psychromonas agarivorans sp. nov., a novel agarolytic bacterium. Int J Syst Evol Microbiol 59:1262–1266

    Article  PubMed  CAS  Google Scholar 

  • Farmer III JJ, Hickman-Brenner FW (2006) The genera Vibrio and Photobacterium. In: The prokaryotes. Springer, New York, pp 508–563

    Chapter  Google Scholar 

  • Ivanova EP, Nedashkovskaya OI, Sawabe T, Zhukova NV, Frolova GM, Nicolau DV, Mikhailov VV, Bowman JP (2004) Shewanella affinis sp. nov., isolated from marine invertebrates. Int J Syst Evol Microbiol 54:1089–1093

    Article  PubMed  CAS  Google Scholar 

  • Ivanova EP, Nedashkovskaya OI, Zhukova NV, Nicolau DV, Christen R, Mikhailov VV (2003) Shewanella waksmanii sp. nov., isolated from a sipuncula (Phascolosoma japonicum). Int J Syst Evol Microbiol 53:1471–1477

    Article  PubMed  CAS  Google Scholar 

  • Ivanova EP, Sawabe T, Gorshkova NM, Svetashev VI, Mikhailov VV, Nicolau DV, Christen R (2001) Shewanella japonica sp. nov. Int J Syst Evol Microbiol 51:1027–1033

    Article  PubMed  CAS  Google Scholar 

  • Jicha GA, Markesbery WR (2010) Omega-3 fatty acids: potential role in the management of early Alzheimer’s disease. Clin Interv Aging 5:45–61

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kahlke T, Thorvaldsen S, Fenton C, Pascarella S, Brettin T (2012) Molecular characterization of cold adaptation of membrane proteins in the Vibrionaceae core-genome. PLoS One 7:e51761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kato C, Nogi Y (2001) Correlation between phylogenetic structure and function: examples from deep-sea Shewanella. FEMS Microbiol Ecol 35:223–230

    Article  PubMed  CAS  Google Scholar 

  • Kautharapu KB, Rathmacher J, Jarboe LR (2013) Growth condition optimization for docosahexaenoic acid (DHA) production by Moritella marina MP-1. Appl Microbiol Biotechnol 97:2859–2866

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto J, Kurihara T, Yamamoto K, Nagayasu M, Tani Y, Mihara H, Hosokawa M, Baba T, Sato SB, Esaki N (2009) Eicosapentaenoic acid plays a beneficial role in membrane organization and cell division of a cold-adapted bacterium, Shewanella livingstonensis Ac10. J Bacteriol 191:632–640

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto J, Sato T, Nakasone K, Kato C, Mihara H, Esaki N, Kurihara T (2011) Favourable effects of eicosapentaenoic acid on the late step of the cell division in a piezophilic bacterium, Shewanella violacea DSS12, at high-hydrostatic pressures. Environ Microbiol 13:2293–2298

    Article  PubMed  CAS  Google Scholar 

  • Kawasaki K, Nogi Y, Hishinuma M, Nodasaka Y, Matsuyama H, Yumoto I (2002) Psychromonas marina sp. nov., a novel halophilic, facultatively psychrophilic bacterium isolated from the coast of the Okhotsk Sea. Int J Syst Evol Microbiol 52:1455–1459

    PubMed  Google Scholar 

  • Kunisawa J, Arita M, Hayasaka T, Harada T, Iwamoto R, Nagasawa R, Shikata S, Nagatake T, Suzuki H, Hashimoto E, Kurashima Y, Suzuki Y, Arai H, Setou M, Kiyono H (2015) Dietary ω3 fatty acid exerts anti-allergic effect through the conversion to 17,18-epoxyeicosatetraenoic acid in the gut. Sci Rep 5:9750

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ledesma-Amaro R, Nicaud J-M (2016) Yarrowia lipolytica as a biotechnological chassis to produce usual and unusual fatty acids. Prog Lipid Res 61:40–50

    Article  PubMed  CAS  Google Scholar 

  • Lee W-H, Cho K-W, Park S-Y, Shin K-S, Lee D-S, Seon-Kap Hwang S-JS (2008a) Identification of psychrophile Shewanella sp. KMG427 as an eicosapentaenoic acid producer. J Microbiol Biotechnol 18:1869–1873

    PubMed  CAS  Google Scholar 

  • Lee S-J, Kim CH, Seo P-S, Kwon O, Hur B-K, Seo J-W (2008b) Enhancement of heterologous production of eicosapentaenoic acid in Escherichia coli by substitution of promoter sequences within the biosynthesis gene cluster. Biotechnol Lett 30:2139–2142

    Article  PubMed  CAS  Google Scholar 

  • Lee SJ, Jeong YS, Kim DU, Se JW, Hur BK (2006) Eicosapentaenoic acid (EPA) biosynthetic gene cluster of Shewanella oneidensis MR-1: cloning, heterologous expression, and effects of temperature and glucose on the production of EPA in Escherichia coli. Biotechnol Bioprocess Eng 11:510–515

    Article  CAS  Google Scholar 

  • Ma D, Seo J, Switzer K, Fan Y, Mcmurray D, Lupton JR, Chapkin RS (2004) n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research. J Nutr Biochem 15:700–706

    Article  PubMed  CAS  Google Scholar 

  • Mandal R, Badyakar D, Chakrabarty J (2014) Role of membrane lipid fatty acids in sperm cryopreservation. Adv Androl 2014:1–9

    Article  Google Scholar 

  • Martinez-Checa F, Béjar V, Llamas I, Del Moral A, Quesada E (2005) Alteromonas hispanica sp. nov., a polyunsaturated-fatty-acid-producing, halophilic bacterium isolated from Fuente de Piedra, southern Spain. Int J Syst Evol Microbiol 55:2385–2390

    Article  PubMed  CAS  Google Scholar 

  • Matsuyama H, Minami H, Sakaki T, Kasahara H, Baba S, Ishimaru S, Hirota K, Yumoto I, Hidetoshi Matsuyama C (2015) Alteromonas gracilis sp. nov., a marine polysaccharide-producing bacterium. Int J Syst Evol Microbiol 65:1498–1503

    Article  PubMed  CAS  Google Scholar 

  • Methé BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang X, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou L, Davidsen TM, Wu M, Huston AL, Lewis M, Weaver B, Weidman JF, Khouri H, Utterback TR, Feldblyum TV, Fraser CM (2005) The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc Natl Acad Sci U S A 102:10913–10918

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Metz JG, Roessler P, Facciotti D, Levering C, Dittrich F, Lassner M, Valentine R, Lardizabal K, Domergue F, Yamada A, Yazawa K, Knauf V, Browse J (2001) Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293:290–293

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki M, Nogi Y, Usami R, Horikoshi K (2006) Shewanella surugensis sp. nov., Shewanella kaireitica sp. nov. and Shewanella abyssi sp. nov., isolated from deep-sea sediments of Suruga Bay, Japan. Int J Syst Evol Microbiol 56:1607–1613

    Article  PubMed  CAS  Google Scholar 

  • Moi IM, Roslan NN, Leow ATC, Ali MSM, Rahman RNZRA, Rahimpour A, Sabri S (2017) The biology and the importance of Photobacterium species. Appl Microbiol Biotechnol 101:4371–4385

    Article  PubMed  CAS  Google Scholar 

  • Morita N, Nishida T, Tanaka M, Yano Y, Okuyama H (2005) Enhancement of polyunsaturated fatty acid production by cerulenin treatment in polyunsaturated fatty acid-producing bacteria. Biotechnol Lett 27:389–393

    Article  PubMed  CAS  Google Scholar 

  • Morita N, Tanaka M, Okuyama H (2000) Biosynthesis of fatty acids in the docosahexaenoic acid-producing bacterium Moritella marina strain MP-1. Biochem Soc Trans 28:943–945

    Article  PubMed  CAS  Google Scholar 

  • Mountfort DO, Rainey FA, Burghardt J, Kaspar HF, Stackebrandt E (1998) Psychromonas antarcticus gen. nov., sp. nov., a new aerotolerant anaerobic, halophilic psychrophile isolated from pond sediment of the McMurdo Ice Shelf, Antarctica. Arch Microbiol 169:231–238

    Article  PubMed  CAS  Google Scholar 

  • Nichols DS, Nichols PD, McMeekin TA (1993) Polyunsaturated fatty acids in Antarctic bacteria. Antarct Sci 5:149–160

    Google Scholar 

  • Nichols PD, Petrie J, Singh S (2010) Long-chain omega-3 oils—an update on sustainable sources. Nutrients 2:572–585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nikoopour H, Griffiths M (2008) Production of EPA by Shewanella putrefaciens MAC1 in selected culture media. http://www.sid.ir/en/VEWSSID/Jpdf/96620080101.pdf

  • Nishida T, Hori R, Morita N, Okuyama H (2010) Membrane eicosapentaenoic acid is involved in the hydrophobicity of bacterial cells and affects the entry of hydrophilic and hydrophobic compounds. FEMS Microbiol Lett 306:91–96

    Article  PubMed  CAS  Google Scholar 

  • Nishida T, Morita N, Yano Y, Orikasa Y, Okuyama H (2007) The antioxidative function of eicosapentaenoic acid in a marine bacterium, Shewanella marinintestina IK-1. FEBS Lett 581:4212–4216

    Article  PubMed  CAS  Google Scholar 

  • Nishida T, Orikasa Y, Watanabe K, Okuyama H (2006) The cell membrane-shielding function of eicosapentaenoic acid for Escherichia coli against exogenously added hydrogen peroxide. FEBS Lett 580:6690–6694

    Article  PubMed  CAS  Google Scholar 

  • Nogi Y (2011) Taxonomy of Psychrophiles. In: Extremophiles handbook. Springer Japan, Tokyo, pp 777–792

    Chapter  Google Scholar 

  • Nogi Y, Hosoya S, Kato C, Horikoshi K (2007) Psychromonas hadalis sp. nov., a novel piezophilic bacterium isolated from the bottom of the Japan Trench. Int J Syst Evol Microbiol 57:1360–1364

    Article  PubMed  CAS  Google Scholar 

  • Nogi Y, Hosoya S, Kato C, Horikoshi K (2004) Colwellia piezophila sp. nov., a novel piezophilic species from deep-sea sediments of the Japan Trench. Int J Syst Evol Microbiol 54:1627–1631

    Article  PubMed  CAS  Google Scholar 

  • Nogi Y, Kato C (1999) Taxonomic studies of extremely barophilic bacteria isolated from the Mariana Trench and description of Moritella yayanosii sp. nov., a new barophilic bacterial isolate. Extremophiles 3:71–77

    Article  PubMed  CAS  Google Scholar 

  • Nogi Y, Kato C, Horikoshi K (1998a) Taxonomic studies of deep-sea barophilic Shewanella strains and description of Shewanella violacea sp. nov. Arch Microbiol 170:331–338

    Article  PubMed  CAS  Google Scholar 

  • Nogi Y, Kato C, Horikoshi K (1998b) Moritella japonica sp. nov., a novel barophilic bacterium isolated from a Japan Trench sediment. J Gen Appl Microbiol 44:289–295

    Article  PubMed  CAS  Google Scholar 

  • Nogi Y, Kato C, Horikoshi K (2002) Psychromonas kaikoae sp. nov., a novel piezophilic bacterium from the deepest cold-seep sediments in the Japan Trench. Int J Syst Evol Microbiol 52:1527–1532

    PubMed  CAS  Google Scholar 

  • Nogi Y, Masui N, Kato C (1998c) Photobacterium profundum sp. nov., a new, moderately barophilic bacterial species isolated from a deep-sea sediment. Extremophiles 2:1–7

    Article  PubMed  CAS  Google Scholar 

  • Okuyama H, Orikasa Y, Nishida T (2008) Significance of antioxidative functions of eicosapentaenoic and docosahexaenoic acids in marine microorganisms. Appl Environ Microbiol 74:570–574

    Article  PubMed  CAS  Google Scholar 

  • Okuyama H, Orikasa Y, Nishida T, Watanabe K, Morita N (2007) Bacterial genes responsible for the biosynthesis of eicosapentaenoic and docosahexaenoic acids and their heterologous expression. Appl Environ Microbiol 73:665–670

    Article  PubMed  CAS  Google Scholar 

  • Orikasa Y, Ito Y, Nishida T, Watanabe K, Morita N, Ohwada T, Okuyama H (2007) Enhanced heterologous production of eicosapentaenoic acid in Escherichia coli cells that co-express eicosapentaenoic acid biosynthesis pfa genes and foreign DNA fragments including a high-performance catalase gene, vktA. Biotechnol Lett 29:803–809

    Article  PubMed  CAS  Google Scholar 

  • Orikasa Y, Nishida T, Yamada A, Yu R, Watanabe K, Hase A, Morita N, Okuyama H (2006) Recombinant production of docosahexaenoic acid in a polyketide biosynthesis mode in Escherichia coli. Biotechnol Lett 28:1841–1847

    Article  PubMed  CAS  Google Scholar 

  • Orikasa Y, Tanaka M, Sugihara S, Hori R, Nishida T, Ueno A, Morita N, Yano Y, Yamamoto K, Shibahara A, Hayashi H, Yamada Y, Yamada A, Yu R, Watanabe K, Okuyama H (2009) PfaB products determine the molecular species produced in bacterial polyunsaturated fatty acid biosynthesis. FEMS Microbiol Lett 295:170–176

    Article  PubMed  CAS  Google Scholar 

  • Orikasa Y, Yamada A, Yu R (2004) Characterization of the eicosapentaenoic acid biosynthesis gene cluster from Shewanella sp. strain SCRC-2738. Cell Mol Biol 50:625–630

    PubMed  CAS  Google Scholar 

  • Park S, Kang C-H, Won S-M, Park J-M, Kim B-C, Yoon J-H, Jung-Hoon Yoon C (2015) Alteromonas confluentis sp. nov., isolated from the junction between the ocean and a freshwater spring. Int J Syst Evol Microbiol 65:3603–3608

    Article  PubMed  CAS  Google Scholar 

  • Peng Y-F, Chen W-C, Xiao K, Xu L, Wang L, Wan X (2016) DHA production in Escherichia coli by expressing reconstituted key genes of polyketide synthase pathway from marine bacteria. PLoS One 11:e0162861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pishva H, Amini M, Eshraghian MR, Hosseini S, Mahboob SA (2012) Effects of EPA supplementation on plasma fatty acids composition in hypertriglyceridemic subjects with FABP2 and PPARα genotypes. J Diabetes Metab Disord 11:1

    Article  CAS  Google Scholar 

  • Raatz SK, Rosenberger TA, Johnson LK, Wolters WW, Burr GS, Picklo MJ (2013) Dose-dependent consumption of farmed Atlantic Salmon (Salmo salar) increases plasma phospholipid n-3 fatty acids differentially. J Acad Nutr Diet 113:282–287

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramakrishnan U, Stein AD, Parra-Cabrera S, Wang M, Imhoff-Kunsch B, Juárez-Márquez S, Rivera J, Martorell R (2010) Effects of docosahexaenoic acid supplementation during pregnancy on gestational age and size at birth: randomized, double-blind, placebo-controlled trial in Mexico. Food Nutr Bull 31:S108–S116

    Article  PubMed  Google Scholar 

  • Rapoport SI, Ramadan E, Basselin M (2011) Docosahexaenoic acid (DHA) incorporation into the brain from plasma, as an in vivo biomarker of brain DHA metabolism and neurotransmission. Prostaglandins Other Lipid Mediat 96:109–113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 86:807–815

    Article  PubMed  CAS  Google Scholar 

  • Ringø E, Sinclair PD, Birkbeck H, Barbour A (1992a) Production of eicosapentaenoic acid (20:5 n-3) by Vibrio pelagius isolated from turbot (Scophthalmus maximus (L.)) larvae. Appl Environ Microbiol 58:3777–3778

    PubMed  PubMed Central  Google Scholar 

  • Ringø E, Jøstensen JP, Olsen RE (1992b) Production of eicosapentaenoic acid by freshwater Vibrio. Lipids 27:564–566

    Article  Google Scholar 

  • Rodríguez-Guilbe M, Oyola-Robles D, Schreiter ER, Baerga-Ortiz A (2013) Structure, activity, and substrate selectivity of the orf6 thioesterase from Photobacterium profundum. J Biol Chem 288:10841–10848

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rubio-Rodríguez N, Beltrán S, Jaime I, de Diego SM, Sanz MT, Carballido JR (2010) Production of omega-3 polyunsaturated fatty acid concentrates. Innovative Food Sci Emerg Technol 11:1–12

  • Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria—a dogma rewritten. Microbiology 145:767–779

    Article  PubMed  CAS  Google Scholar 

  • Sakuradani E, Ando A, Shimizu S, Ogawa J (2013) Metabolic engineering for the production of polyunsaturated fatty acids by oleaginous fungus Mortierella alpina 1S-4. J Biosci Bioeng 116:417–422

    Article  PubMed  CAS  Google Scholar 

  • Sato SB, Park J, Kawamoto J, Sato S, Kurihara T (2013) Inhibition of constitutive Akt (PKB) phosphorylation by docosahexaenoic acid in the human breast cancer cell line MDA-MB-453. Biochim Biophys Acta Mol Cell Biol Lipids 1831:306–313

    Article  CAS  Google Scholar 

  • Schober ME (2016) Docosahexaenoic acid and omega-3 fatty acids. In: New therapeutics for traumatic brain injury: prevention of secondary brain damage and enhancement of repair and regeneration, p 287

  • Seo HJ, Bae SS, Lee JH, Kim SJ (2005) Photobacterium frigidiphilum sp. nov., a psychrophilic, lipolytic bacterium isolated from deep-sea sediments of Edison Seamount. Int J Syst Evol Microbiol 55:1661–1666

    Article  PubMed  CAS  Google Scholar 

  • Shulse CN, Allen EE (2011) Widespread occurrence of secondary lipid biosynthesis potential in microbial lineages. PLoS One 6:e20146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Siriwardhana N, Kalupahana NS, Moustaid-Moussa N (2012) Health benefits of n-3 polyunsaturated fatty acids: eicosapentaenoic acid and docosahexaenoic acid. Adv Food Nutr Res 65:211–222

    Article  PubMed  Google Scholar 

  • Skerratt JH, Bowman JP, Nichols PD (2002) Shewanella olleyana sp. nov., a marine species isolated from a temperate estuary which produces high levels of polyunsaturated fatty acids. Int J Syst Evol Microbiol 52:2101–2106

    PubMed  CAS  Google Scholar 

  • Sugihara S, Orikasa Y, Okuyama H (2008) An EntD-like phosphopantetheinyl transferase gene from Photobacterium profundum SS9 complements pfa genes of Moritella marina strain MP-1 involved in biosynthesis of docosahexaenoic acid. Biotechnol Lett 30:411–414

    Article  PubMed  CAS  Google Scholar 

  • Swanson D, Block R, Mousa SA (2012) Omega-3 fatty acids EPA and DHA: health benefits throughout life. Adv Nutr An Int Rev J 3:1–7

    Article  CAS  Google Scholar 

  • Takeyama H, Takeda D, Yazawa K, Yamada A, Matsunaga T (1997) Expression of the eicosapentaenoic acid synthesis gene cluster from Shewanella sp. in a transgenic marine cyanobacterium, Synechococcus sp. Microbiology 143:2725–2731

    Article  PubMed  CAS  Google Scholar 

  • Tanaka M, Ueno A, Kawasaki K, Yumoto I, Ohgiya S, Hoshino T, Ishizaki K, Okuyama H, Morita N (1999) Isolation of clustered genes that are notably homologous to the eicosapentaenoic acid biosynthesis gene cluster from the docosahexaenoic acid-producing bacterium Vibrio marinus strain MP-1. Biotechnol Lett 21:939–945

    Article  CAS  Google Scholar 

  • Tilay A, Annapure U (2012) Novel simplified and rapid method for screening and isolation of polyunsaturated fatty acids producing marine bacteria. Biotechnol Res Int 2012:1–8

    Article  CAS  Google Scholar 

  • Urakawa H, Yoshida T, Nishimura M, Ohwada K (2000) Characterization of depth-related population variation in microbial communities of a coastal marine sediment using 16S rDNA-based approaches and quinone profiling. Environ Microbiol 2:542–554

    Article  PubMed  CAS  Google Scholar 

  • Usui K, Hiraki T, Kawamoto J, Kurihara T, Nogi Y, Kato C, Abe F (2012) Eicosapentaenoic acid plays a role in stabilizing dynamic membrane structure in the deep-sea piezophile Shewanella violacea: a study employing high-pressure time-resolved fluorescence anisotropy measurement. Biochim Biophys Acta Biomembr 1818:574–583

    Article  CAS  Google Scholar 

  • van den Elsen L, Garssen J, Willemsen L (2012) Long chain N-3 polyunsaturated fatty acids in the prevention of allergic and cardiovascular disease. Curr Pharm Des 18:2375–2392

    Article  PubMed  Google Scholar 

  • Van Landschoot A, De ley J (1983) Intra- and intergeneric similarities of the rRNA cistrons of Alteromonas, Marinomonas (gen. nov.) and some other Gram-negative bacteria. Microbiology 129:3057–3074

    Article  Google Scholar 

  • Van Trappen S, Tan T-L, Yang J, Mergaert J, Swings J (2004) Alteromonas stellipolaris sp. nov., a novel, budding, prosthecate bacterium from Antarctic seas, and emended description of the genus Alteromonas. Int J Syst Evol Microbiol 54:1157–1163

    Article  PubMed  CAS  Google Scholar 

  • Voigt RG, Jensen CL, Fraley JK, Rozelle JC, Brown FR, Heird WC (2002) Relationship between omega 3 long-chain polyunsaturated fatty acid status during early infancy and neurodevelopmental status at 1 year of age. J Hum Nutr Diet 15:111–120

    Article  PubMed  CAS  Google Scholar 

  • Wallis JG, Watts JL, Browse J (2002) Polyunsaturated fatty acid synthesis: what will they think of next? Trends Biochem Sci 27:467–473

    Article  PubMed  CAS  Google Scholar 

  • Wan X, Peng Y-F, Zhou X-R, Gong Y-M, Huang F-H, Moncalián G (2016) Effect of cerulenin on fatty acid composition and gene expression pattern of DHA-producing strain Colwellia psychrerythraea strain 34H. Microb Cell Factories 15:30

    Article  CAS  Google Scholar 

  • Wang F, Wang P, Chen M, Xiao X (2004) Isolation of extremophiles with the detection and retrieval of Shewanella strains in deep-sea sediments from the West Pacific. Extremophiles 8:165–168

    Article  PubMed  CAS  Google Scholar 

  • Wang F, Xiao X, Ou H-Y, Gai Y, Wang F (2009) Role and regulation of fatty acid biosynthesis in the response of Shewanella piezotolerans WP3 to different temperatures and pressures. J Bacteriol 191:2574–2584

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiao X, Wang P, Zeng X, Bartlett DH, Wang F (2007) Shewanella psychrophila sp. nov. and Shewanella piezotolerans sp. nov., isolated from West Pacific deep-sea sediment. Int J Syst Evol Microbiol 57:60–65

    Article  PubMed  CAS  Google Scholar 

  • Xie D, Jackson EN, Zhu Q (2015) Sustainable source of omega-3 eicosapentaenoic acid from metabolically engineered Yarrowia lipolytica: from fundamental research to commercial production. Appl Microbiol Biotechnol 99:1599–1610

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu Y, Nogi Y, Kato C, Liang Z, Rüger H-J, De KD, Glansdorff N (2003) Moritella profunda sp. nov. and Moritella abyssi sp. nov., two psychropiezophilic organisms isolated from deep Atlantic sediments. Int J Syst Evol Microbiol 53:533–538

    Article  PubMed  CAS  Google Scholar 

  • Xue Z, Sharpe PL, Hong S-P, Yadav NS, Xie D, Short DR, Damude HG, Rupert RA, Seip JE, Wang J, Pollak DW, Bostick MW, Bosak MD, Macool DJ, Hollerbach DH, Zhang H, Arcilla DM, Bledsoe SA, Croker K, McCord EF, Tyreus BD, Jackson EN, Zhu Q (2013) Production of omega-3 eicosapentaenoic acid by metabolic engineering of Yarrowia lipolytica. Nat Biotechnol 31:734–740

    Article  PubMed  CAS  Google Scholar 

  • Yang S-H, Lee J-H, Ryu J-S, Kato C, Kim S-J (2007) Shewanella donghaensis sp. nov., a psychrophilic, piezosensitive bacterium producing high levels of polyunsaturated fatty acid, isolated from deep-sea sediments. Int J Syst Evol Microbiol 57:208–212

    Article  PubMed  CAS  Google Scholar 

  • Yazawa K (1996) Production of eicosapentaenoic acid from marine bacteria. Lipids 31(Suppl):S297–S300

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama M, Origasa H, Matsuzaki M, Matsuzawa Y, Saito Y, Ishikawa Y, Oikawa S, Sasaki J, Hishida H, Itakura H, Kita T, Kitabatake A, Nakaya N, Sakata T, Shimada K, Shirato K, Japan EPA lipid intervention study (JELIS) Investigators (2007) Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomised open-label, blinded endpoint analysis. Lancet 369:1090–1098

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Hashimoto M, Hori R, Adachi T, Okuyama H, Orikasa Y, Nagamine T, Shimizu S, Ueno A, Morita N (2016) Bacterial long-chain polyunsaturated fatty acids: their biosynthetic genes, functions, and practical use. Mar Drugs 14:94

    Article  PubMed Central  CAS  Google Scholar 

  • Yu R, Yamada A, Watanabe K, Yazawa K, Takeyama H, Matsunaga T, Kurane R (2000) Production of eicosapentaenoic acid by a recombinant marine cyanobacterium, Synechococcus sp. Lipids 35:1061–1064

    Article  PubMed  CAS  Google Scholar 

  • Zhang D-C, Yu Y, Xin Y-H, Liu H-C, Zhou P-J, Zhou Y-G (2008) Colwellia polaris sp. nov., a psychrotolerant bacterium isolated from Arctic sea ice. Int J Syst Evol Microbiol 58:1931–1934

    Article  PubMed  CAS  Google Scholar 

  • Zhao J-S, Manno D, Leggiadro C, O’Neil D, Hawari J (2006) Shewanella halifaxensis sp. nov., a novel obligately respiratory and denitrifying psychrophile. Int J Syst Evol Microbiol 56:205–212

    Article  PubMed  CAS  Google Scholar 

  • Zhu Q, Jackson EN (2015) Metabolic engineering of Yarrowia lipolytica for industrial applications. Curr Opin Biotechnol 36:65–72

    Article  PubMed  CAS  Google Scholar 

  • Zulyniak MA, Perreault M, Gerling C, Spriet LL, Mutch DM (2013) Fish oil supplementation alters circulating eicosanoid concentrations in young healthy men. Metabolism 62:1107–1113

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Syazwan Ngalimat for his help on the figures.

Funding

This study was funded by research grant number 02-02-14-1500FR under the Fundamental Research Grant Scheme (FRGS) from the Ministry of Higher Education, Government of Malaysia.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suriana Sabri.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moi, I.M., Leow, A.T.C., Ali, M.S.M. et al. Polyunsaturated fatty acids in marine bacteria and strategies to enhance their production. Appl Microbiol Biotechnol 102, 5811–5826 (2018). https://doi.org/10.1007/s00253-018-9063-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-9063-9

Keywords

Navigation