Skip to main content

Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

Abstract

Contamination of sediments with crude oil promotes the growth of different species of phototrophs and heterotrophs. The coexistence of these two groups in oil-polluted sites suggested a possible contribution to hydrocarbon degradation; however, the exact role and interactions between phototrophs and heterotrophs in the degradation processes have only been recently evaluated. Experiments with axenic and non-axenic cultures of phototrophs suggested that they were unable to degrade hydrocarbons and degradation was mostly attributed to their associated heterotrophs. As primary producers, phototrophs do not have an innate potential for hydrocarbon degradation but can be engaged in symbiosis with oil-degrading heterotrophs. The degradation of hydrocarbons by the associated aerobic heterotrophs can promote the growth of phototrophs by reducing the concentrations of potentially toxic hydrocarbons around them, regenerating CO2 for photosynthesis, providing metabolites, and reducing the high toxic concentrations of O2. On the other hand, phototrophs can support the activity of oil-degrading heterotrophs by immobilizing them in their sheaths, providing them with O2 and fixed nitrogen (in the case of cyanobacteria), and directly supplying them with necessary organics produced by their photosynthetic and fermentation activities. It is concluded that phototrophs and heterotrophs constitute ideal consortia that are efficient in the decontamination of oil-polluted sites, compared to individual organisms. However, further research is required to find out the species specificity and the chemical substances that govern the exact relationship and interaction between phototrophs and heterotrophs.

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

Access this chapter

Institutional subscriptions

References

  • Abed RMM (2010) Interaction between cyanobacteria and aerobic heterotrophic bacteria in the degradation of hydrocarbons. Int Biodeterior Biodegrad 64:58–64

    Article  CAS  Google Scholar 

  • Abed RMM, Golubic S (2009) Selection of oil-tolerant cyanobacteria on oil polluted sediments. Algol Stud 130:89–99

    Article  Google Scholar 

  • Abed RMM, Köster J (2005) The direct role of aerobic heterotrophic bacteria associated with cyanobacteria in the degradation of oil compounds. Int Biodeterior Biodegrad 55:29–37

    Article  CAS  Google Scholar 

  • Abed RMM, Safi NMD, Köster J, de Beer D, Rullkötter J, Garcia-Pichel F (2002) Microbial diversity of a heavily polluted microbial mat and its community changes following degradation of petroleum compounds. Appl Environ Microbiol 68:1674–1683

    Article  CAS  Google Scholar 

  • Abed RMM, Kohls K, de Beer D (2007) Effect of salinity changes on the bacterial diversity, photosynthesis and oxygen consumption of cyanobacterial mats from an intertidal flat of the Arabian Gulf. Environ Microbiol 9:1384–1392

    Article  CAS  Google Scholar 

  • Abed RMM, Musat N, Musat F, Mußmann M (2011) Structure of microbial communities and hydrocarbon-dependent sulfate reduction in the anoxic layer of a polluted microbial mat. Mar Pollut Bull 62:539–546

    Article  CAS  Google Scholar 

  • Al-Hadhrami MN, Lappin-Scott HM, Fisher PJ (1996) Effects of the addition of organic carbon sources on bacterial respiration and n-alkane biodegradation of Omani crude oil. Mar Pollut Bull 32:351–357

    Article  CAS  Google Scholar 

  • Al-Hasan RH, Al-Bader DA, Sorkhoh NA, Radwan SS (1998) Evidence of n-alkane consumption and oxidation by filamentous cyanobacteria from oil-contaminated coasts of the Arabian Gulf. Mar Biol 130:521–527

    Article  CAS  Google Scholar 

  • Al-Hasan RH, Khanfar M, Eliyas M, Radwan SS (2001) Hydrocarbon accumulation by picocyanobacteria from the Arabian Gulf. J Appl Microbiol 91:533–540

    Article  CAS  Google Scholar 

  • Amin SA, Parker MS, Armbrust EV (2012) Interactions between diatoms and bacteria. Microbiol Mol Biol Rev 76(3):667–684

    Article  CAS  Google Scholar 

  • Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522(7554):98–101

    Article  CAS  Google Scholar 

  • Anderson KL, Tayne TA, Ward DM (1987) Formation and fate of fermentation products in hot-spring cyanobacterial mats. Appl Environ Microbiol 53:2343–2352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baines SB, Pace ML (1991) The production of dissolved organic matter by phytoplankton and its importance to bacteria: pattern across marine and freshwater systems. Limnol Oceanogr 36:1078–1090

    Article  Google Scholar 

  • Barth JJ (2003) The influence of cyanobacteria on oil polluted intertidal soils at the Saudi Arabian Gulf shores. Mar Pollut Bull 46:1245–1252

    Article  CAS  Google Scholar 

  • Bateson MM, Ward DM (1988) Photoexcretion and fate of glycolate in a hot spring cyanobacterial mat. Appl Environ Microbiol 54:1738–1743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Batterton J, Winters K, Baalen CV (1978) Sensitivity of three microalgae to crude oils and fuel oils. Mar Environ Res 1:31–41

    Article  CAS  Google Scholar 

  • Bauld J, Brock TD (1974) Algal excretion and bacterial assimilation in hot spring algal mats. J Phycol 10:101–106

    Google Scholar 

  • Behrens S, Losekann T, Pett-Ridge J, Weber PK, Ng WO, Stevenson BS, Hutcheon ID, Relman DA, Spormann AM (2008) Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl Environ Microbiol 74:3143–3150

    Article  CAS  Google Scholar 

  • Belyaev SS, Laurinavichus KS, Obratsova SN, Gorlatov SN, Ivanov MV (1982) Microbiological processes in the critical zone of injection wells in oilfields. Microbiol (Transl. from Mikrobiologiya, Moscow) 51:793–797

    Google Scholar 

  • Benthien M, Wieland A, de Oteyza TG, Grimalt JO, Kühl M (2004) Oil contamination effects on a hypersaline microbial mat community (Camargue, France) as studied with microsensors and geochemical analysis. Ophelia 58:135–150

    Article  Google Scholar 

  • Bragg GR, Prince RC, Harner EJ, Atlas RM (1994) Effectiveness of bioremediation for the Exxon Valdez oil spill. Nature 368:413–418

    Article  CAS  Google Scholar 

  • Burkholder PR (1963) Some nutritional relationships among microbes of sea sediments and waters. In: Oppenheimer CH (ed) Symposium on marine microbiology. C.C. Thomas, Springfield, pp 133–150

    Google Scholar 

  • Cerniglia CE, Baalen CV, Gibson DT (1980a) Metabolism of naphthalene by the cyanobacterium Oscillatoria sp., strain JCM. J Gen Microbiol 116:485–494

    CAS  Google Scholar 

  • Cerniglia CE, Gibson DT, Baalen CV (1980b) Oxidation of naphthalene by cyanobacteria and microalgae. J Gen Microbiol 116:495–500

    CAS  Google Scholar 

  • Chaillan F, Gugger M, Saliot A, Coute A, Oudot J (2006) Role of cyanobacteria in biodegradation of crude oil by a tropical cyanobacterial mat. Chemosphere 62:1574–1582

    Article  CAS  Google Scholar 

  • Chen YP, Lopez-de-Victoria G, Lovell CR (1993) Utilization of aromatic compounds as carbon and energy sources during growth and N2-fixation by free living nitrogen fixing bacteria. Arch Microbiol 159:207–212

    Article  CAS  Google Scholar 

  • Chronopoulou P-M, Fahy A, Coulon F, Paissé S, Goñi-Urriza MS, Peperzak L, Acuña Alvarez L, McKew BA, Lawson T, Timmis KN, Duran R, Underwood GJC, McGenity TJ (2013) Impact of a simulated oil spill on benthic phototrophs and nitrogen-fixing bacteria. Environ Microbiol 15:241–252

    Article  Google Scholar 

  • Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13:291–314

    Article  Google Scholar 

  • Cooper MB, Smith AG (2015) Exploring mutualistic interactions between microalgae and bacteria in the omic age. Curr Opin Plant Biol 26:147–153

    Article  Google Scholar 

  • Coulon F, Chronoupolou P-M, Fahy A, Païssé S, Goñi-Urriza MS, Peperzak L, Acuña Alvarez L, McKew BA, Brussard C, Underwood GJC, Timmis KN, Duran R, McGenity TJ (2012) Central role of dynamic tidal biofilms dominated by aerobic hydrocarbonoclastic bacteria and diatoms in the biodegradation of hydrocarbons in coastal mudflats. Appl Environ Microbiol 78:3638–3648

    Article  CAS  Google Scholar 

  • Decho A (1990) Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanogr Mar Biol Annu Rev 28:73–153

    Google Scholar 

  • Ellis BE (1977) Degradation of phenolic compounds by fresh water algae. Plant Sci Lett 8:213–216

    Article  CAS  Google Scholar 

  • Epping EHG, Khalili A, Thar R (1999) Dynamics of photosynthesis and respiration in an intertidal biofilm. Limnol Oceanogr 44:1936–1948

    Article  Google Scholar 

  • Fitzsimons AG, Smith RV (1984) The isolation and growth of axenic cultures of planktonic blue-green algae. Br Phycol J 19:156–162

    Article  Google Scholar 

  • Flemming HC, Wingender J (2001) Relevance of microbial extrapolymeric substances (EPSs)-Part I: structural and ecological aspects. Water Sci Technol 43:1–8

    Article  CAS  Google Scholar 

  • Gamila HA, Ibrahim MBM (2004) Algal bioassay for evaluating the role of algae in bioremediation of crude oil: I-isolated strains. Bull Environ Contam Toxicol 73:883–889

    Article  CAS  Google Scholar 

  • Garcia-Pichel F, Kühl M, Nübel U, Muyzer G (1999) Salinity dependent limitation of photosynthesis and oxygen exchange in microbial mats. J Phycol 35:184–195

    Article  Google Scholar 

  • Headly JV, Du JL, Peru KM, Gurprasad N, McMartin DW (2008) Evaluation of algal phytodegradation of petroleum naphthenic acids. J Environ Sci Health A 43:227–232

    Article  Google Scholar 

  • Hellebust J (1965) Excretion of some organic compounds by marine phytoplankton. Limnol Oceanogr 10:192–206

    Article  Google Scholar 

  • Herbst V, Overbeck J (1978) Metabolic coupling between the alga Oscillatoria redekei and accompanying bacteria. Naturwissenschaften 65:598–599

    Article  CAS  Google Scholar 

  • Hoffmann L (1996) Recolonization of the intertidal flats by microbial mats after the Gulf War oil spill. In: Krupp F, Abduzinada AH, Nader IA (eds) A marine wildlife sanctuary for the Arabian Gulf: environmental research and conservation following the 1991 Gulf War oil spill. Senkenberg Research Institute/NCWCD, Riyad/Frankfurt, pp 96–115

    Google Scholar 

  • Höpner T, Yousef M, Berthe-Corti L, Felzmann H, Struck H, Al-Thukair A (1996) Cyanobacterial mats on oil-polluted sediments–start of a promising self-remediation process? In: Krupp F, Abuzinada AH, Nader IA (eds) A marine wildlife sanctuary for the Arabian Gulf: environmental research and conservation following the 1991 Gulf War oil spill. NCWCD/Senckenberg Research Institute, Riyadh/Frankfurt, pp 85–95

    Google Scholar 

  • Jonkers HM, Abed RMM (2003) Identification of aerobic heterotrophic bacteria from the photic zone of a hypersaline microbial mat. Aquat Microb Ecol 30:127–133

    Article  Google Scholar 

  • Jørgensen BB, Nelson DC, Ward DM (1992) Chemotrophy and decomposition in modern microbial mats. In: Schopf JW, Klein C (eds) The proterozoic biosphere: a multidisciplinary study. Cambridge University Press, Cambridge, pp 287–293

    Google Scholar 

  • Kirkwood AE, Nalewajko C, Fulthorpe RR (2006) The effects of cyanobacterial exudates on bacterial growth and biodegradation of organic contaminants, Microb Ecol 51:4–12

    Article  CAS  Google Scholar 

  • Kouzuma A, Watanabe K (2015) Exploring the potential of algae-bacteria interactions. COBiotech 33:125–129

    CAS  Google Scholar 

  • Lange W (1967) Effect of carbohydrates on the symbiotic growth of planktonic blue-green algae with bacteria. Nature 215:1277–1278

    Article  CAS  Google Scholar 

  • Lea-Smith DJ, Biller SJ, Davey MP, Cotton CAR, Perez Sepulveda BM, 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 USA 112:13591–13596

    Article  CAS  Google Scholar 

  • Lee K, Tremblay GH, Cobanli SE (1995) Bioremediation of oiled beach sediments: assessment of inorganic and organic fertilizers. In: Proceedings of the 1991 oil spill conference. American Petroleum Institute, Washington, DC, pp 107–113

    Google Scholar 

  • Liu A, Zhu T, Lu X, Song L (2013) Hydrocarbon profiles and phylogenetic analyses of diversified cyanobacterial species. Appl Energy 111:383–393

    Article  CAS  Google Scholar 

  • McGenity TJ, Folwell BD, McKew BA, Sanni GO (2012) Marine crude-oil biodegradation: a central role for interspecies interactions. Aquatic Biosyst 8:10

    Article  Google Scholar 

  • Megharaj M, Singleton I, McClure NC, Naidu R (2000) Influence of petroleum hydrocarbon contamination on microalgae and microbial activities in a long-term contaminated soil. Arch Environ Contam Toxicol 38:439–445

    Article  CAS  Google Scholar 

  • Munoz R, Guieysse B, Mattiasson B (2003) Phenanthrene biodegradation by an algal bacterium consortium in two phase partitioning bioreactors. Appl Microbiol Biotechnol 61:261–267

    Article  CAS  Google Scholar 

  • Musat F, Wieland A, Widdel F (2004) Marine sediment with surface contamination by oil in microcosms for microbiological studies. Ophelia 58:217–222

    Article  Google Scholar 

  • Musat F, Harder J, Widdel F (2006) Study of nitrogen fixation in microbial communities of oil-contaminated marine sediment microcosms. Environ Microbiol 8:1834–1843

    Article  CAS  Google Scholar 

  • Narro ML (1985) Oxidation of aromatic hydrocarbons by marine cyanobacteria. PhD thesis, The university of Texas at Austin, Austin

    Google Scholar 

  • Narro ML (1987) Petroleum toxicity and the oxidation of aromatic hydrocarbons. In: Fay P, Baalen CV (eds) The cyanobacteria. Elsevier, Amsterdam, pp 493–511

    Google Scholar 

  • Nazina TN, Rozanova EP, Kuznetsov SI (1985) Microbial oil transformation processes accompanied by methane and hydrogen sulfide formation. Geomicrobiol J 4:103–130

    Article  CAS  Google Scholar 

  • Nold SC, Ward DM (1996) Photosynthate partitioning and fermentation in hot spring microbial mat communities. Appl Environ Microbiol 62:4598–4607

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Brien PY, Dixon PS (1976) The effects of oil and oil components on algae: a review. Br Phycol J 11:115–142

    Article  Google Scholar 

  • Paerl HW (1976) Specific association of the blue-green algae Anabaena and Aphanizomenon with bacteria in freshwater bloom. J Phycol 12:431–435

    Google Scholar 

  • Paerl HW (1982) Interactions with bacteria. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Botanical monographs. Blackwell, Oxford, pp 241–462

    Google Scholar 

  • Paerl HW, Bebout BM, Joye SB, Des Marais DJ (1993) Microscale characterization of dissolved organic-matter production and uptake in marine microbial mat communities. Limnol Oceanogr 38:1150–1161

    Article  CAS  Google Scholar 

  • Pett-Ridge J, Weber PK (2012) NanoSIP: NanoSIMS applications for microbial ecology. Methods Mol Biol 881:375–408. https://doi.org/10.1007/978-1-61779-827-6_13

    Article  CAS  PubMed  Google Scholar 

  • Prantera MT, Drozdowicz A, Leite SG, Rosado AS (2002) Degradation of gasoline hydrocarbons by two N2-fixing soil bacteria. Biotechnol Lett 24:85–89

    Article  CAS  Google Scholar 

  • Prince RC (2018) Eukaryotic hydrocarbon degraders. In: McGenity TJ (ed) Taxonomy, genomics and ecophysiology of hydrocarbon-degrading microbes. Handbook of hydrocarbon and lipid microbiology. Springer. https://doi.org/10.1007/978-3-319-60053-6_16-1

    Google Scholar 

  • Radwan SS, Al-Hasan RH (2000) Oil pollution and cyanobacteria. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer, Dordrecht, pp 307–319

    Google Scholar 

  • Radwan SS, Al-Awandhi H, Sorkhoh NA, El-Nemr IM (1998) Rhizospheric hydrocarbon utilizing microorganisms as potential contributors to phytoremediation for the oily Kuwaiti desert. Microbiol Res 153:247–251

    Article  CAS  Google Scholar 

  • Radwan SS, Al-Aawadi HA, Khanafer M (2001) Effects of lipids on n-alkane attenuation in media supporting oil utilizing microorganisms from the oily Arabian Gulf coasts. FEMS Microbiol Lett 198:99–103

    Article  CAS  Google Scholar 

  • Radwan SS, Al-Hasan RH, Salamah S, Al-Dabbous S (2002) Bioremediation of oily sea water by bacteria immobilized in biofilms coating macroalgae. Int Biodeterior Biodegrad 50:55–59

    Article  CAS  Google Scholar 

  • Raghukumar C, Vipparty V, David JJ, Chandramohan D (2001) Degradation of crude oil by marine cyanobacteria. Appl Microbiol Biotechnol 57:433–436

    Article  CAS  Google Scholar 

  • Ramanan R, Kim B-H, Cho D-H, Oh H-M, Kim H-S (2016) Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29

    Article  CAS  Google Scholar 

  • Rippka R (1988) Isolation and purification of cyanobacteria. In: Packer L, Glazer AN (eds) Methods in enzymology: cyanobacteria. Academic, New York, pp 3–27

    Chapter  Google Scholar 

  • Rivet L, Mille G, Basseres A, Ladousse A, Gerin C, Acquaviva M, Bertrand J-C (1993) n alkane biodegradation by a marine bacterium in the presence of an oleophilic nutriment. Biotechnol Lett 15:637–640

    Article  CAS  Google Scholar 

  • Rosenberg E, Legmann R, Kushmaro A, Taube R, Adler E, Ron EZ (1992) Petroleum bioremediation – a multiphase problem. Biodegradation 3:337–350

    Article  CAS  Google Scholar 

  • Safonova ET, Dmitrieva IA, Kvitko KV (1999) The interaction of algae with alcanotrophic bacteria in black oil decomposition. Resour Conserv Recycl 27:193–201

    Article  Google Scholar 

  • Sanchez O, Diestra E, Esteve I, Mas J (2005) Molecular characterization of an oil-degrading cyanobacterial consortium. Microb Ecol 50:580–588

    Article  CAS  Google Scholar 

  • Sanchez O, Ferrera I, Vigues N, de Oteyza TG, Grimalt J, Mas J (2006) Role of cyanobacteria in oil biodegradation by microbial mats. Int Biodeterior Biodegrad 58:186–195

    Article  CAS  Google Scholar 

  • Sorkhoh N, Al-Hasan R, Radwan S (1992) Self-cleaning of the Gulf. Nature 359:109

    Article  Google Scholar 

  • Sorkhoh NA, Al-Hasan RH, Khanafer M, Radwan SS (1995) Establishment of oil degrading bacteria associated with cyanobacteria in oil-polluted soil. J Appl Bacteriol 78:194–199

    Article  CAS  Google Scholar 

  • Stal LJ (1995) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol 131:1–32

    Article  CAS  Google Scholar 

  • Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS Microbiol Rev 21(179):211

    Google Scholar 

  • Steppe TF, Olson JB, Paerl HW, Litaker RW, Belnap J (1996) Consortial N2 fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats. FEMS Microbiol Ecol 21:149–156

    Article  CAS  Google Scholar 

  • Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkatewarlu K, Naidu R (2011) Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol Adv 29:896–907

    Article  CAS  Google Scholar 

  • Tang X, He LY, Tao XQ, Dang Z, Guo CL, Lu GN, Yi XY (2010) Construction of an artificial microalgal-bacterial consortium that efficiently degrades crude oil. J Hazard Mater 181:1158–1162

    Article  CAS  Google Scholar 

  • Vandermeulen JH, Ahem TP (1976) Effect of petroleum hydrocarbons on the algal physiology: review and progress report. In: Lockwood APM (ed) Effects of pollution on aquatic organisms. Cambridge University Press, London, pp 107–125

    Google Scholar 

  • Vidyashankar S, Ravishankar GA (2016) Algae-based bioremediation: bioproducts and biofuels for biobusiness. In: Prasad MNV (ed) Bioremediation and bioeconomy. Elsevier, Amsterdam, pp 457–483

    Chapter  Google Scholar 

  • Walker JD, Colwell RR, Vaituzis Z, Meyer SA (1975) Petroleum-degrading achlorophyllous alga Prototheca zopfii. Nature (London) 254:423–424

    Article  CAS  Google Scholar 

  • Wang L, Priscu JC (1994) Stimulation of aquatic bacterial activity by cyanobacteria. Hydrobiologia 277:145–158

    Article  Google Scholar 

  • Whitton BA (1973) In: Carr NG, Whitton BA (eds) The biology of blue-green algae. 9. Blackwell Scientific, Oxford/London/Edinburg/Melbourne, pp 353–367

    Google Scholar 

  • Wieland A, Kühl M (2006) Regulation of photosynthesis and oxygen consumption in a hypersaline cyanobacterial mat (Camargue, France) by irradiance, temperature and salinity. FEMS Microbiol Ecol 55:195–210

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raeid M. M. Abed .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this entry

Check for updates. Verify currency and authenticity via CrossMark

Cite this entry

Abed, R.M.M. (2019). Phototroph-Heterotroph Oil-Degrading Partnerships. In: McGenity, T. (eds) Microbial Communities Utilizing Hydrocarbons and Lipids: Members, Metagenomics and Ecophysiology . Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-60063-5_15-1

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-60063-5_15-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-60063-5

  • Online ISBN: 978-3-319-60063-5

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics