Biodiversity of polycyclic aromatic hydrocarbon‐degrading bacteria from deep sea sediments of the Middle Atlantic Ridge

Abstract

Summary The bacteria involved in the biodegradation of polycyclic aromatic hydrocarbons (PAHs) in deep sea subsurface environments are largely unknown. In order to reveal their biodiversity, sediments from 2.2 m under the bottom surface at a water depth of 3542 m were sampled on the Middle Atlantic Ridge with a gravity column sampler. The sediments were promptly enriched with either crude oil or a mixture of PAHs (naphthalene, phenanthrene and pyrene) as the sole carbon source, and further enriched with the PAH mixture mentioned above in the lab. The resulting consortia were named C2CO and C2PPN respectively. Their bacterial composition was analysed with plate cultivation, PCR‐DGGE and 16S rDNA library analysis. On plates, isolates belonging to Pseudoalteromonas , Halomonas , Marinobacter , Thalassospira and Tistrella dominated the culturable populations. With PCR‐DGGE, five major bands closely related to Cycloclasticus , Alteromonas , Thalassospira , Alcanivorax and Rhodospirillaceae were detected in consortium C2CO, while only one major band of Cycloclasticus was detected in consortium C2PPN. In addition, the dynamics of community structure in response to aromatic substrate alterations were examined. As a result, three ribotypes of Cycloclasticus were detected by 16S rDNA library analysis, one which played a key role in phenanthrene degradation; two Alteromonas bacteria dominated the naphthalene reselected consortium. Although bacteria of the two genera grew as the main members of the communities, none of them were isolated, probably owing to their poor cultivability. These results confirm that bacteria of Cycloclasticus are important obligate PAH degraders in marine environments, and coexist with other degrading bacteria that inhabit the deep subsurface sediment of the Atlantic. This supports the view that PAH accumulation and bioattenuation occur in remote areas consistently and continuously.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 42

1. 1.

   Bartlett D, Douglas HB. Microbial adaptation to the psychrosphere/piezosphere. Molecular Marine Microbiology. 2000;185-202.

   Not in our library

2. 2.

   Bull AT, Ward AC, Goodfellow M. Search and discovery strategies for biotechnology: the paradigm shift. Microbiol Mol Biol Rev. 2000;64:573-606.

   Not in our library10.1128/mmbr.64.3.573-606.2000

3. 3.

   Calvo C, Martínez-Checa F, Toledo F, Porcel J, Quesada E. Characteristics of bioemulsifiers synthesised in crude oil media by Halomonas eurihalina and their effectiveness in the isolation of bacteria able to grow in the presence of hydrocarbons. Appl Microbiol Biotech. 2002;60:347-351.

   Not in our library10.1007/s00253-002-1115-4

4. 4.

   Chung WK, King GM. Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description of Lutibacterium anuloederans gen. nov., sp. nov., and Cycloclasticus spirillensus sp. nov. Appl Environ Microbiol. 2001;67:5585-5592.

   Not in our library10.1128/aem.67.12.5585-5592.2001

5. 5.

   Coulon F, McKew BA, Osborn AM, McGenity TJ, Timmis KN. Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol. 2007;9:177-186.

   Not in our library10.1111/j.1462-2920.2006.01126.x

6. 6.

   Demaneche S, Meyer C, Micoud J, Louwagie M, Willison JC, Jouanneau Y. Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol. 2004;70:6714-6725.

   Not in our library10.1128/aem.70.11.6714-6725.2004

7. 7.

   Deming JW. Deep ocean environmental biotechnology. Curr Opin Biotechnol. 1998;9:283-287.

   Not in our library10.1016/s0958-1669(98)80060-8

8. 8.

   Dyksterhouse SE, Gray JP, Herwig RP, Lara JC, Staley JT. Cycloclasticus pugetii gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium from marine sediments. Int J Syst Bacteriol. 1995;45:116-123.

   Not in our library10.1099/00207713-45-1-116

9. 9.

   Escartin E, Porte C. Hydroxylated PAHs in bile of deepsea fish. Relationship with xenobiotic metabolizing enzymes. Environ Sci Technol. 1999;33:2710-2714.

   Not in our library

10. 10.

    Foustoukos DI, Seyfried WE. Hydrocarbons in hydrothermal vent fluids: the role of chromium-bearing catalysts. Science. 2004;304:1002-1005.

    Not in our library10.1126/science.1096033

11. 11.

    Garcia MT, Ventosa A, Mellado E. Catabolic versatility of aromatic compound-degrading halophilic bacteria. FEMS Microbiol Ecol. 2005;54:97-109.

    Not in our library10.1016/j.femsec.2005.03.009

12. 12.

    Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P, Bertrand JC. Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new extremely halotolerant, hydrocarbondegrading marine bacterium. Int J Syst Bacteriol. 1992;42:568-576.

    Not in our library10.1099/00207713-42-4-568

13. 13.

    Gilewicz M, Ni'matuzahroh T, Nadalig H, Budzinski P, Doumenq V, Michotey JC, Bertrand JC. Isolation and characterization of a marine bacterium capable of utilizing 2-methylphenanthrene. Appl Microbiol Biotechnol. 1997;48:528-533.

    Not in our library10.1007/s002530051091

14. 14.

    Head IM, Jones DM, Röling WFM. Marine microorganisms make a meal of oil. Nat Rev Microbiol. 2006;4:173-182.

    Not in our library10.1038/nrmicro1348

15. 15.

    Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT. Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov. Appl Environ Microbiol. 1999;65:251-259.

    Not in our library10.1128/aem.65.1.251-259.1999

16. 16.

    Holm NG, Charlou JL. Initial indications of abiotic formation of hydrocarbons in the rainbow ultramafic hydrothermal system, Mid-Atlantic Ridge. Earth Planet Sci Lett. 2001;191:1-8.

    Not in our library

17. 17.

    Karinen JF. Petroleum in the deep sea environment: potential for damage to biota. Environ Int. 1980;3:135-144.

    Not in our library

18. 18.

    Kasai Y, Kishira H, Harayama S. Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment. Appl Environ Microbiol. 2002;68:5625-5633.

    Not in our library10.1128/aem.68.11.5625-5633.2002

19. 19.

    Kato C, Qureshi MH, Horikoshi K, Douglas HB. Pressure response in deep-sea piezophhilic bacteria. Molecular Marine Microbiology. 2000;185-202.

    Not in our library

20. 20.

    Kazunga C, Michael DA. Products from the incomplete metabolism of pyrene by polycyclic aromatic hydrocarbon-degrading bacteria. Appl Environ Microbiol. 2000;66:1917-1922.

    Not in our library10.1128/aem.66.5.1917-1922.2000

21. 21.

    Kennish MJ, Kennish MJ. Chapter 4. Marine geology. Practical Handbook of Marine Science. 2000;279-439.

    Not in our library

22. 22.

    Liang Y, Tsea MF, Young L, Wong MH. Distribution patterns of polycyclic aromatic hydrocarbons (PAHs) in the sediments and fish at Mai Po Marshes Nature Reserve, Hong Kong. Wat Res. 2007;41:1303-1311.

    Not in our library10.1016/j.watres.2006.11.048

23. 23.

    Lipiatou E, Tolosa I, Simo R, Bouloubassi I, Dachs J, Marti S, et al. Mass budget and dynamics of polycyclic aromatic hydrocarbons in the Mediterranean sea. Deep-Sea Res II. 1997;44:881-905.

    Not in our library

24. 24.

    Liu CL, Shao ZZ. Alcanivorax dieselolei sp. nov., a novel alkane-degrading bacterium isolated from sea water and deep-sea sediment. Int J Syst Evol Microbiol. 2005;55:1181-1186.

    Not in our library10.1099/ijs.0.63443-0

25. 25.

    McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ. Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol. 2007a;9:165-176.

    Not in our library10.1111/j.1462-2920.2006.01125.x

26. 26.

    McKew BA, Coulon F, Yakimov MM, Denaro R, Genovese M, Smith CJ, et al. Efficacy of intervention strategies for bioremediation of crude oil in marine systems and effects on indigenous hydrocarbonoclastic bacteria. Environ Microbiol. 2007b;9:1562-1571.

    Not in our library10.1111/j.1462-2920.2007.01277.x

27. 27.

    Maruyama A, Ishiwata H, Kitmmura K, Sunamura M, Fujita T, Matsuo M, Higashihara T. Dynamics of microbial populations and strong selection for Cycloclasticus pugetii following the Nakhodka oil spill. Microb Ecol. 2003;46:442-453.

    Not in our library10.1007/s00248-002-3010-z

28. 28.

    Melcher RJ, Apitz SE, Hemmingsen BB. Impact of irradiation and polycyclic aromatic hydrocarbon spiking on microbial populations in marine sediment for future aging and biodegradability studies. Appl Environ Microbiol. 2002;68:2858-2868.

    Not in our library10.1128/aem.68.6.2858-2868.2002

29. 29.

    Muyzer G, De Waal EC, Uitterlinden AG. Profiling of complex microbial populations by denaturing gradient gel electrophoresisanalysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol. 1993;59:695-700.

    Not in our library10.1128/aem.59.3.695-700.1993

30. 30.

    Okpokwasili GC, Somerville CC, Grimes DJ, Colwell RR. Plasmid-associated phenanthrene degradation by Chesapeake Bay sediment bacteria. Colloq Institute Fr Rech Explort March. 1984;3:601-610.

    Not in our library

31. 31.

    Porte C, Escartin E, Garcia LM, Sole M, Albaiges J. Xenobiotic metabolising enzymes and antioxidant defences in deep-sea fish: relationship with contaminant body burden. Mar Ecol Prog Ser. 2000;192:259-266.

    Not in our library

32. 32.

    Proskurowski G, Lilley MD, Seewald JS, Früh-Green GL, Olson EJ, Lupton JE, et al. Abiogenic hydrocarbon production at lost city hydrothermal field. Science. 2008;319:604-607.

    Not in our library10.1126/science.1151194

33. 33.

    Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: a Laboratory Manual. 1989.

    Not in our library

34. 34.

    Schwarz JR, Walker JD, Colwell RR. Deep-sea bacteria: growth and utilization of hydrocarbons at ambient and in situ pressure. Appl Microbiol. 1974a;28:982-986.

    Not in our library10.1128/am.28.6.982-986.1974

35. 35.

    Schwarz JR, Walker JD, Colwell RR. Growth of deep-sea bacteria on hydrocarbons at ambient and in situ pressure. Dev Ind Microbiol. 1974b;15:239-249.

    Not in our library10.1128/am.28.6.982-986.1974

36. 36.

    Simoneit BRT. Petroleum generation, an easy and widespread process in hydrothermal system: an overview. Appl Geochem. 1990;5:17-18.

    Not in our library

37. 37.

    Steimle FW, Zdanowicz VS, Gadbois DF. Metals and organic contaminants in Northwest Atlantic deep-sea tilefish tissues. Mar Pollut Bull. 1990;21:530-535.

    Not in our library

38. 38.

    Wang BJ, Lai QL, Cui ZS, Tan TF, Shao ZZ. A pyrene-degrading consortium from deep-sea sediment of the west pacific and its key member Cycloclasticus sp. P1. Environ Microbiol.

    Not in our library10.1111/j.1462-2920.2008.01611.x

39. 39.

    West PA, Okpokwasili GC, Colwell PR. Numerical taxonomy of phenanthrene-degrading bacteria isolated from Chesapeake Bay. Appl Environ Microbiol. 1984;48:988-993.

    Not in our library10.1128/aem.48.5.988-993.1984

40. 40.

    Woodwell GM, Craig PP, Johnson HJ. DDT in the biosphere: where does it go? Science. 1971;174:1101-1107.

    Not in our library10.1126/science.174.4014.1101

41. 41.

    Yakimov MM, Golyshin PN, Lang S, Moore ER, Abraham WR, Lunsdorf H, Timmis KN. Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol. 1998;48:339-348.

    Not in our library10.1099/00207713-48-2-339

42. 42.

    Yoon JH, Kim IG, Kang KH, Oh TK, Park YH. Alteromonas marina sp. nov., isolated from sea water of the east sea in Korea. Int J Syst Evol Microbiol. 2003;53:1625-1630.

    Not in our library10.1099/ijs.0.02536-0

Cited by papers we hold 2

• Current State of Knowledge in Microbial Degradation of Polycyclic Aromatic Hydrocarbons (PAHs): A Review · 2016
  Corrected
• Marine crude-oil biodegradation: a central role for interspecies interactions · 2012
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.