Conversion of Uric Acid into Ammonium in Oil-Degrading Marine Microbial Communities: a Possible Role of Halomonads
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Uric acid is a promising hydrophobic nitrogen source for biostimulation of microbial activities in oil-impacted marine environments. This study investigated metabolic processes and microbial community changes in a series of microcosms using sediment from the Mediterranean and the Red Sea amended with ammonium and uric acid. Respiration, emulsification, ammonium and protein concentration measurements suggested a rapid production of ammonium from uric acid accompanied by the development of microbial communities containing hydrocarbonoclastic bacteria after 3 weeks of incubation. About 80 % of uric acid was converted to ammonium within the first few days of the experiment. Microbial population dynamics were investigated by Ribosomal Intergenic Spacer Analysis and Illumina sequencing as well as by culture-based techniques. Resulting data indicated that strains related to Halomonas spp. converted uric acid into ammonium, which stimulated growth of microbial consortia dominated by Alcanivorax spp. and Pseudomonas spp. Several strains of Halomonas spp. were isolated on uric acid as the sole carbon source showed location specificity. These results point towards a possible role of halomonads in the conversion of uric acid to ammonium utilized by hydrocarbonoclastic bacteria.
KeywordsCrude oil degradation Bioremediation Alcanivorax
The authors would like to thank Anna Foster, Sarah Chesworth and Gordon Turner for their help with photometric and respiration measurements. With exception of XH and JC, all authors were supported by the FP7 Project ULIXES (FP7-KBBE-2010-266473). This work was further funded by grant BIO2011-25012 from the Spanish Ministry of the Economy and Competitiveness. FM was supported by Università degli Studi di Milano, European Social Fund (FSE) and Regione Lombardia (contract “Dote Ricerca”). DD acknowledges support of KAUST, King Abdullah University of Science and Technology. PG acknowledges the support of the European Commission through the project Kill-Spill (FP7, Contract Nr 312139). CG would like to thank Mr. Kyungsun Lee of Macrogen Inc. for his courtesy regarding sequencing services, J. Cans, B. Strid and C. Hudson for continued advice and inspiration as well as Delphine Lallias for her help with multivariate statistics and John Flannery for proofreading this manuscript.
- 3.Atlas EL (1975) Phosphate equilibria in seawater and interstitial waters. PhD thesis. Oregon State Univ., Corvallis, Oregon.Google Scholar
- 5.Capone DG, Bronk DA, Mulholland MR & Carpenter EJ (2008) Nitrogen in the marine environment. (Academic Press, 2008). at http://www.sciencedirect.com/science/book/9780123725226.
- 7.Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
- 9.Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver SpringsGoogle Scholar
- 13.Garcia HE, Locarnini RA, Boyer TP, Antonov JI, Zweng MM, Baranova OK & Johnson DR (2010) World Ocean Atlas 2009, Volume 4: Nutrients (phosphate, nitrate, silicate). S. Levitus, Ed. NOAA Atlas NESDIS 71, U.S. Government Printing Office, Washington, D.C.Google Scholar
- 19.Hammer Ø, Harper DAT, Ryan PD (2001) PAST: palaeontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
- 29.Kube M, Chernikova TN, Al-Ramahi Y, Beloqui A, Lopez-Cortez N, Guazzaroni ME, Heipieper HJ, Klages S, Kotsyurbenko OR, Langer I, Nechitaylo TY, Lünsdorf H, Fernández M, Juárez S, Ciordia S, Singer A, Kagan O, Egorova O, Petit PA, StogiosP KY, Tchigvintsev A, Flick R, Denaro R, Genovese M, Albar JP, Reva ON, Martínez-Gomariz M, Tran H, Ferrer M, Savchenko A, Yakunin AF, Yakimov MM, Golyshina OV, Reinhardt R, Golyshin PN (2013) Genome sequence and functional genomics analysis of the oil-degrading bacterium Oleispira antarctica. Nat Commun 4:2156PubMedCentralCrossRefPubMedGoogle Scholar
- 39.Mulvaney, R. (1996) in Methods of soil analysis part 3: chemical methods. 1123–1184 Soil Science Society of America, Inc.Google Scholar
- 41.Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
- 49.Wang Z, Hollebone BP, Fingas M, Fieldhouse B, Sigouin L, Landriault M, SmithP, Noonan J & Thouin G (2003) Characteristics of spilled oils, fuels, and petroleum products: 1. Composition and properties of selected oils. United States Environmental Protection Agency, National Exposure Research Laboratory, EPA/600/R-03/072Google Scholar
- 51.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 49:419–432CrossRefPubMedGoogle Scholar