Naphthalene biodegradation in temperate and arctic marine microcosms

Biodegradation

Volumn 25, Issue 1, 2014, Pages 111-125

  Bagi, Andrea ^a   Pampanin, Daniela M ^b   Lanzén, Anders ^c   Bilstad, Torleiv ^a   Kommedal, Roald ^a  

^a UNIVERSITY OF STAVANGER   (Norway)

^b INTERNATIONAL RESEARCH INSTITUTE OF STAVANGER   (Norway)

^c UNIVERSITY OF BERGEN   (Norway)

Author keywords

Biodegradation; DGGE; Hydrocarbons; Naphthalene; Pyrosequencing; Q10; Seawater

Indexed keywords

BACTERIAL COMMUNITY COMPOSITION; DGGE; ENVIRONMENTAL RISK ASSESSMENT; NAPHTHALENE BIODEGRADATION; POLYCYCLIC AROMATIC HYDROCARBON (PAH); POLYMERASE CHAIN REACTION-DENATURING GRADIENT GEL ELECTROPHORESIS; PYROSEQUENCING; Q10;

CLIMATE MODELS; DEGRADATION; ELECTROPHORESIS; HYDROCARBONS; MICROBIOLOGY; NAPHTHALENE; OIL SPILLS; POLYCYCLIC AROMATIC HYDROCARBONS; POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SEAWATER;

BIODEGRADATION;

ARCTIC ENVIRONMENT; BIODEGRADATION; ENVIRONMENTAL FATE; ENVIRONMENTAL RISK; MARINE ENVIRONMENT; MARINE POLLUTION; MICROBIAL COMMUNITY; MICROCOSM; NAPHTHALENE; NUMERICAL MODEL; OIL SPILL; OXYGEN CONSUMPTION; PAH; POLLUTANT REMOVAL; POLLUTANT SOURCE; POLYMERASE CHAIN REACTION; SEAWATER; TEMPERATE ENVIRONMENT;

ARCTIC OCEAN; ATLANTIC OCEAN; NORTH SEA;

BACTERIA (MICROORGANISMS);

NAPHTHALENE; NAPHTHALENE DERIVATIVE; PETROLEUM; RNA 16S; SEA WATER;

ARCTIC; ARTICLE; BACTERIUM; BIOREMEDIATION; CLASSIFICATION; COLD; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA SEQUENCE; ECOSYSTEM; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL CONSORTIUM; MICROBIOLOGY; NORTH SEA; PHYLOGENY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; WATER POLLUTANT;

ARCTIC REGIONS; BACTERIA; BIODEGRADATION, ENVIRONMENTAL; COLD TEMPERATURE; DENATURING GRADIENT GEL ELECTROPHORESIS; ECOSYSTEM; MICROBIAL CONSORTIA; NAPHTHALENES; NORTH SEA; PETROLEUM; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; WATER POLLUTANTS, CHEMICAL;

EID: 84892436465     PISSN: 09239820     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10532-013-9644-3     Document Type: Article

References (70)

1. Ahn IS, Ghiorse WC, Lion LW, Shuler ML (1998) Growth kinetics of Pseudomonas putida G7 on naphthalene and occurrence of naphthalene toxicity during nutrient deprivation. Biotechnol Bioeng 59(5): 587-594. doi: 10. 1002/(SICI)1097-0290(19980905)59: 5<587: AID-BIT9>3. 0. CO;2-6.
2. Arnosti C, Jørgensen BB, Sagemann J, Thamdrup B (1998) Temperature dependence of microbial degradation of organic matter in marine sediments: polysaccharide hydrolysis, oxygen consumption, and sulfate reduction. Mar Ecol Prog Ser 165: 59-70.
3. Arrhenius S (1889) Über die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durch Sauren. Zeitschrift für Physik Chemie 4: 226-248.
4. Atlas RM (1975) Effects of temperature and crude oil composition on petroleum biodegradation. Appl Microbiol 30(3): 396-403.
5. Atlas RM (1981) Microbial degradation of petroleum hydrocarbons: an environmental perspective. Microbiol Rev 45(1): 180-209.
6. Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens: reevaluation of a unique biological group. Microbiol Rev 43(2): 260-296.
7. Bano N, Hollibaugh JT (2002) Phylogenetic composition of bacterioplankton assemblages from the Arctic Ocean. Appl Environ Microbiol 68(2): 505-518. doi: 10. 1128/AEM. 68. 2. 505-518. 2002.
8. Bauer JE, Capone DG (1985) Degradation and mineralization of the polycyclic aromatic hydrocarbons anthracene and naphthalene in intertidal marine sediment. Appl Environ Microbiol 50(1): 81-90.
9. Brakstad OG (2008) Natural and stimulated biodegradation of petroleum in cold marine Environments. In: Margesin R, Schinner F, Marx J-C, Gerday C (eds) Psychrophiles: from biodiversity to biotechnology. Springer, Berlin, pp 389-407.
10. Brakstad OG, Bonaunet K (2006) Biodegradation of petroleum hydrocarbons in seawater at low temperatures (0-5 °C) and bacterial communities associated with degradation. Biodegradation 17(1): 71-82. doi: 10. 1007/s10532-005-3342-8.
11. Brakstad OG, Faksness L-G (2000) Biodegradation of water-accommodated fractions and dispersed oil in the seawater column. In: Proceedings to the SPE Conference on Health, Safety and Environment in Oil and Gas Exploration and Production, 26-28 June 2000, Stavanger, Norway. Society for Petroleum Engineers (SPE) Paper 61466.
12. Brakstad OG, Bonaunet K, Nordtug T, Johansen Ø (2004) Biotransformation and dissolution of petroleum hydrocarbons in natural flowing seawater at low temperature. Biodegradation 15(5): 337-346.
13. Brakstad OG, Nonstad I, Faksness L-G, Brandvik PJ (2008) Responses of microbial communities in Arctic sea ice after contamination by crude petroleum oil. Microb Ecol 55(3): 540-552. doi: 10. 1007/s00248-007-9299-x.
14. Brakstad OG, Booth AM, Faksness L-G, Aislabie J (2009) Microbial degradation of petroleum compounds in cold marine water and ice. In: Bej AK, Atlas RM (eds) Polar microbiology: the ecology, biodiversity and bioremediation potential of microorganisms in extremely cold environments. CRC Press, New York, pp 231-253.
15. Brauer VS, de Jonge VN, Buma AGJ, Weissing FJ (2009) Does universal temperature dependence apply to communities? An experimental test using natural marine plankton assemblages. Oikos 118: 1102-1108. doi: 10. 1111/j. 1600-0706. 2009. 17371. x.
16. Castle DM, Montgomery MT, Kirchman DL (2006) Effects of naphthalene on microbial community composition in the Delaware estuary. FEMS Microbiol Ecol 56(1): 55-63. doi: 10. 1111/j. 1574-6941. 2006. 00062. x.
17. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3: 351-368.
18. Chablain PA, Philippe G, Groboillot A, Truffaut N, Guespin-Michel JF (1997) Isolation of soil psychrotrophic toluene-degrading Pseudomonas strain: influence of temperature on the growth characteristics on different substrates. Res Microbiol 148(2): 153-161.
19. Chao A (1987) Estimating the population size for capture-recaprure data with unequal catchability. Biometrics 43(4): 783-791.
20. Courtes R, Bahlaoui A, Rambaud A, Deschamps F, Sunde E, Dutrieux E (1995) Ready biodegradability test in seawater: a new methodological approach. Ecotoxicol Environ Saf 31(2): 142-148.
21. D'Amico S, Collins T, Marx J-C, Feller G, Gerday C (2006) Psychrophilic microorganisms: challenges for life. EMBO Rep 7: 385-389. doi: 10. 1038/sj. embor. 7400662.
22. Delille D, Pelletier E, Rodriguez-Blanco A, Ghiglione J-F (2009) Effects of nutrient and temperature on degradation of petroleum hydrocarbons in sub-Antarctic coastal seawater. Polar Biol 32(10): 1521-1528. doi: 10. 1007/s00300-009-0652-z.
23. Deppe U, Richnow H-H, Michaelis W, Antranikian G (2005) Degradation of crude oil by an arctic microbial consortium. Extremophiles 9(6): 461-470. doi: 10. 1007/s00792-005-0463-2.
24. Feller G, Gerday C (2003) Psychrophilic enzymes: hot topics in cold adaptation. Nat Rev Microbiol 1(3): 200-208. doi: 10. 1038/nrmicro773.
25. Feng J, Ellis L (2012) Benzoate pathway. University of Minnesota biocatalysis biodegradation database. http://umbbd. ethz. ch/benz2/benz2_map. html. Accessed 29 Nov 2012.
26. Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S (2006) Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Nat Acad Sci USA 103(35): 13104-13109. doi: 103: 13104-13109.
27. Fuhrman JA, Steele JA, Hewson I, Schwalbach MS, Brown MV, Green JL, Brown JH (2008) A latitudinal diversity gradient in planktonic marine bacteria. Proc Nat Acad Sci USA 105(22): 7774-7778. doi: 105: 7774-7778.
28. Geiselbrecht AD, Hedlund BP, Tichi MA, Staley JT (1998) Isolation of marine polycyclic aromatic hydrocarbon (PAH)-degrading Cycloclasticus strains from the Gulf of Mexico and comparison of their PAH degradation ability with that of Puget Sound Cycloclasticus strains. Appl Environ Microbiol 64(12): 4703-4710.
29. Gibbs CF, Pugh KB, Andrews AR (1975) Quantitative studies on marine biodegradation of oil II. Effect of temperature. Proc R Soc Lond B 188(1090): 83-94. doi: 10. 1098/rspb. 1975. 0004.
30. Giebel HA, Kalhoefer D, Lemke A, Thole S, Gahl-Janssen R, Simon M, Brinkhoff T (2011) Distribution of Roseobacter RCA and SAR11 lineages in the North Sea and characteristics of an abundant RCA isolate. ISME J 5(1): 8-19.
31. Gilbert JA, Steele JA, Caporaso JG, Steinbru L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Join I, Somerfield P, Fuhrman JA, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6: 298-308. doi: 10. 1038/ismej. 2011. 107.
32. Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293(5538): 2248-2251. doi: 10. 1126/science. 1061967.
33. Gold G, Rodriguez S (1988) The effect of temperature and salinity on the Setschenow parameters of naphthalene in seawater. Can J Chem 67(5): 822-826. doi: 10. 1139/v89-127.
34. Heitkamp MA, Freeman JP, Cerniglia CE (1987) Naphthalene biodegradation in environmental microcosms: estimates of degradation rates and characterization of metabolites. Appl Environ Microbiol 53(1): 129-136.
35. 10 of soil respiration in sub-alpine Australia reflect influences of vegetation types. Soil Biol Biochem 43(6): 1266-1274. doi: 10. 1016/j. soilbio. 2011. 02. 017.
36. Karhu M, Kaakinen J, Kuokkanen T, Rämö J (2009) Biodegradation of light fuel oils in water and soil as determined by the manometric respirometry method. Water Air Soil Pollut 197(1-4): 3-14. doi: 10. 1007/s11270-008-9752-6.
37. Kirchman DL (2008) Microbial ecology of the oceans, 2nd edn. Wiley, Hoboken, ISBN: 978-0-470-04344-8.
38. Knoblauch C, Jørgensen BB, Harder J (1999) Community size and metabolic rates of psychrophilic sulfate reducing bacteria in Arctic marine sediments. Appl Environ Microbiol 65(9): 4230-4233.
39. Kuokkanen T, Vähäoja P, Välimäki I, Lauhanen R (2004) Suitability of the respirometric BOD oxitop method for determining the biodegradability of oils in ground water using forestry hydraulic oils as model compounds. Intern J Environ Anal Chem 84(9): 677-689. doi: 10. 1080/03067310410001688435.
40. Lanzén A, Jørgensen SL, Huson DH, Gorfer M, Grindhaug SH, Jonassen I, Øvreås L, Urich T (2012) CREST-classification resources for environmental sequence tags. PLoS ONE 7(11): e49334. doi: 10. 1371/journal. pone. 0049334.
41. Latimer JS, Zheng J (2003) The sources, transport, and fate of PAHs in the marine environment. In: Douben PET (ed) PAHs: an ecotoxicological perspective, 1st edn. Wiley, West Sussex. doi: 10. 1002/0470867132. ch2.
42. Lauro FM, Allen MA, Wilkins D, Williams TJ, Cavicchioli R (2011) Psychrophiles: genetics, genomics, evolution. In: Horikochi K, Antranikian G, Bull AT, Robb FT, Stetter KO (eds) Extremophiles handbook, 1st edn. Springer, Tokyo, pp 865-891.
43. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54(3): 305-315.
44. McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary UK. Environ Microbiol 9(1): 165-176. doi: 10. 1111/j. 1462-2920. 2006. 01125. x.
45. Methe BA, Nelson KE, Deming JW, Momen B, Melamud E, Zhang XJ, Moult J, Madupu R, Nelson WC, Dodson RJ, Brinkac LM, Daugherty SC, Durkin AS, DeBoy RT, Kolonay JF, Sullivan SA, Zhou LW, 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 Nat Acad Sci USA 102(31): 10913-10918. doi: 10. 1073/pnas. 0504766102.
46. Michaud L, Lo Giudice A, Saitta M, De Domenico M, Bruni V (2004) The biodegradation efficiency on diesel oil by two psychrotrophic Antarctic marine bacteria during a two-month-long experiment. Mar Pollut Bull 49(5-6): 405-409. doi: 10. 1016/j. marpolbul. 2004. 02. 026.
47. Minas W, Gunkel W (1995) Oil pollution in the North Sea-a microbiological point of view. Helgoländer Meeresuntersuchungen 49(1-4): 143-158. doi: 10. 1007/BF02368345.
48. Moore MN, Livingstone DR, Widdows J (1989) Hydrocarbons in marine mollusks: biological effects and ecological consequences. In: Varanasi U (ed) Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment. CRC Press Inc., Boca Raton, pp 291-328.
49. Niepceron M, Portet-Koltalo F, Merlin C, Motelay-Massei A, Barray S, Bodilis J (2009) Both Cycloclasticus spp. and Pseudomonas spp. as PAH-degrading bacteria in the Seine estuary (France). FEMS Microbiol Ecol 37(1): 137-147. doi: 10. 1111/j. 1574-6941. 2009. 00832. x.
50. OECD (1992) OECD Guidelines for testing of chemicals/section 3: degradation and accumulation. Test number 306: biodgradability in seawater. OECD publishing, Paris, ISBN: 9789264070486.
51. Pampanin DM, Sydnes MO (2013) Polycyclic aromatic hydrocarbons a constituent of petroleum: Presence and influence in the aquatic environment. In: Vladimir K, Kolesnikov A (eds) Hydrocarbon. InTech, Rijeka, ISBN 978-953-51-0927-3.
52. Price PB, Sowers T (2004) Temperature dependence of metabolic rates for microbial growth, maintenance, and survival. Proc Nat Acad Sci USA 101(13): 4631-4636. doi: 10. 1073pnas. 0400522101.
53. Quince C, Curtis TP, Sloan WT (2008) The rational exploration of microbial diversity. The ISME Journal 2: 997-1006. doi: 10. 1038/ismej. 2008. 69.
54. Quince C, Lanzén A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38. doi: 10. 1186/1471-2105-12-38.
55. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, ISBN 3-900051-07-0, http://www. R-project. org.
56. Reed M, Johansen Ø, Brandvik PJ, Daling P, Lewis A, Fiocco R, Mackay D, Prentki R (1999) Oil spill modeling towards the close of the 20th century: overview of the state of the art. Spill Sci Technol Bull 5(1): 3-16.
57. Reed M, Singsass I, Daling PS, Faksness L-G, Brakstad OG, Hetland B, Hokstad J (2001) Modelling the water-accomodated fraction in OSCAR2000. Proceedings of 2001 International Oil Spill Conference. Tampa.
58. Robador A, Bruchert V, Jørgensen BB (2009) The impact of temperature change on the activity and community composition of sulfate-reducing bacteria in arctic versus temperate marine sediments. Environ Microbiol 11(7): 1692-1703. doi: 10. 1111/j. 1462-2920. 2009. 01896. x.
59. Røberg S, Østerhus JI, Landfald B (2011) Dynamics of bacterial community exposed to hydrocarbons and oleophilic fertilizer in high-Arctic intertidal beach. Polar Biol 34(10): 1455-1465. doi: 10. 1007/s00300-011-1003-4.
60. Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana.
61. Siron R, Pelletier É, Brochu C (1995) Environmental factors influencing the biodegradation of petroleum hydrocarbons in cold seawater. Arch Environ Contam Toxicol 28: 406-416. doi: 10. 1007/BF00211621.
62. Stewart PS, Tedaldi DJ, Lewis AR, Goldman E (1993) Biodegradation rates of crude oil in seawater. Water Environ Res 65(7): 845-848.
63. Valentine DL, Mezic I, Macesic S, Crnjaric-Zic N, Ivic S, Hogan PJ, Fonoberov VA, Loire S (2012) Dynamic autoinoculation and the microbial ecology of a deep water hydrocarbon irruption. Proc Nat Acad Sci USA. doi: 10. 1073/pnas. 1108820109.
64. van Stempvoort D, Biggar K (2008) Potential for bioremediation of petroleum hydrocarbons in groundwater under cold climate conditions: a review. Cold Regions Sci Tech 53(1): 16-41. doi: 10. 1016/j. coldregions. 2007. 06. 009.
65. 10 relationship of microbial respiration in a temperate forest soil. Soil Biol Biochem 28(8): 1067-1072.
66. Yakimov MM, Gentile G, Bruni V, Cappello S, D'Auria G, Golyshin PN, Giuliano L (2004) Crude oil-induced structural shift of coastal bacterial communities of rod bay (Terra Nova Bay, Ross Sea, Antarctica) and characterization of cultured cold-adapted hydrocarbonoclastic bacteria. FEMS Microbiol Ecol 49(3): 419-432. doi: 10. 1016/j. femsec. 2004. 04. 018.
67. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotech 18(3): 257-266. doi: 10. 1016/j. copbio. 2007. 04. 006.
68. Zeng Y, Essenberg C (2011) Naphthalene pathway map. University of Minnesota biocatalysis biodegradation database. http://umbbd. ethz. ch/naph/naph_map. html. Accessed 29 Nov 2012.
69. Zobell CE (1946) Action of microorganisms on hydrocarbons. Bacteriol Rev 10(1-2): 1-49.
70. Zobell CE, Grant CW, Haas HF (1943) Marine microorganisms which oxidize petroleum hydrocarbons. AAPG Bull 27(9): 1175-1193.