Effect of energy deprivation on metabolite release by anaerobic marine naphthalene-degrading sulfate-reducing bacteria.


Journal

Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692

Informations de publication

Date de publication:
09 2020
Historique:
received: 07 05 2020
revised: 02 08 2020
accepted: 09 08 2020
pubmed: 13 8 2020
medline: 7 4 2021
entrez: 13 8 2020
Statut: ppublish

Résumé

The aromatic hydrocarbon naphthalene, which occurs in coal and oil, can be degraded by aerobic or anaerobic microorganisms. A wide-spread electron acceptor for the latter is sulfate. Evidence for in situ naphthalene degradation stems in particular from the detection of 2-naphthoate and [5,6,7,8]-tetrahydro-2-naphthoate in oil field samples. Because such intermediates are usually not detected in laboratory cultures with high sulfate concentrations, one may suppose that conditions in reservoirs, such as sulfate limitation, trigger metabolite release. Indeed, if naphthalene-grown cells of marine sulfate-reducing Deltaproteobacteria (strains NaphS2, NaphS3 and NaphS6) were transferred to sulfate-free medium, they released 2-naphthoate and [5,6,7,8]-tetrahydro-2-naphthoate while still consuming naphthalene. With 2-naphthoate as initial substrate, cells produced [5,6,7,8]-tetrahydro-2-naphthoate and the hydrocarbon, naphthalene, indicating reversibility of the initial naphthalene-metabolizing reaction. The reactions in the absence of sulfate were not coupled to observable growth. Excretion of naphthalene-derived metabolites was also achieved in sulfate-rich medium upon addition of the protonophore carbonyl cyanide4-(trifluoromethoxy)phenylhydrazone or the ATPase inhibitor N,N'-dicyclohexylcarbodiimide. In conclusion, obstruction of electron flow and energy gain by sulfate limitation offers an explanation for the occurrence of naphthalene-derived metabolites in oil reservoirs, and provides a simple experimental tool for gaining insights into the anaerobic naphthalene oxidation pathway from an energetic perspective.

Identifiants

pubmed: 32783260
doi: 10.1111/1462-2920.15195
doi:

Substances chimiques

Culture Media 0
Fossil Fuels 0
Naphthalenes 0
Sulfates 0
naphthalene 2166IN72UN
2-naphthoic acid QLG01V0W2L

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4057-4066

Subventions

Organisme : Max-Planck-Gesellschaft
Pays : International

Informations de copyright

© 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.

Références

Aitken, C.M., Jones, D.M., and Larter, S.R. (2004) Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs. Nature 431: 291-294.
Azuma, H., Toyota, M., Asakawa, Y., and Kawano, S. (1996) Naphthalene-a constituent of Magnolia flowers. Phytochemistry 42: 999-1004.
Bar-Even, A., Flamholz, A., Noor, E., and Milo, R. (2012) Thermodynamic constraints shape the structure of carbon fixation pathways. Biochim Biophys Acta 1817: 1646-1659.
Bedessem, M.E., Swoboda-Colberg, N.G., and Colberg, P.J.S. (1997) Naphthalene mineralization coupled to sulfate reduction in aquifer-derived enrichments. FEMS Microbiol Lett 152: 213-218.
Bergmann, F.D., Selesi, D., and Meckenstock, R.U. (2011) Identification of new enzymes potentially involved in anaerobic naphthalene degradation by the sulfate-reducing enrichment culture N47. Arch Microbiol 193: 241-250.
Boronin, A.M., and Kosheleva, I.A. (2010) Diversity of naphthalene biodegradation systems in soil bacteria. In Handbook of Hydrocarbon and Lipid Microbiology, Timmis, K.N. (ed). Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 1155-1163.
Chang, W., Um, Y., and Holoman, T.R.P. (2006) Polycyclic aromatic hydrocarbon (PAH) degradation coupled to methanogenesis. Biotechnol Lett 28: 425-430.
Chen, J., Henderson, G., Grimm, C.C., Lloyd, S.W., and Laine, R.A. (1998) Termites fumigate their nests with naphthalene. Nature 392: 558-559.
Coates, J.D., Woodward, J., Allen, J., Philp, P., and Lovley, D.R. (1997) Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbor sediments. Appl Environ Microbiol 63: 3589-3593.
Cord-Ruwisch, R. (1985) A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. J Microbiol Methods 4: 33-36.
Daisy, B.H., Strobel, G.A., Castillo, U., Ezra, D., Sears, J., Weaver, D.K., and Runyon, J.B. (2002) Naphthalene, an insect repellent, is produced by Muscodor vitigenus, a novel endophytic fungus. Microbiology-SGM 148: 3737-3741.
DiDonato, R.J., Jr., Young, N.D., Butler, J.E., Chin, K.-J., Hixson, K.K., Mouser, P. et al. (2010) Genome sequence of the Deltaproteobacterial strain NaphS2 and analysis of differential gene expression during anaerobic growth on naphthalene. Plos One 5: e14072.
Dimroth, P., and Hilpert, W. (1984) Carboxylation of pyruvate and acetyl coenzyme a by reversal of the Na+ pumps oxaloacetate decarboxylase and methylmalonyl-CoA decarboxylase. Biochemistry 23: 5360-5366.
Dimroth, P., and Schink, B. (1998) Energy conservation in the decarboxylation of dicarboxylic acids by fermenting bacteria. Arch Microbiol 170: 69-77.
Eberlein, C., Estelmann, S., Seifert, J., von Bergen, M., Muller, M., Meckenstock, R.U., and Boll, M. (2013a) Identification and characterization of 2-naphthoyl-coenzyme A reductase, the prototype of a novel class of dearomatizing reductases. Mol Microbiol 88: 1032-1039.
Eberlein, C., Johannes, J., Mouttaki, H., Sadeghi, M., Golding, B.T., Boll, M., and Meckenstock, R.U. (2013b) ATP-dependent/-independent enzymatic ring reductions involved in the anaerobic catabolism of naphthalene. Environ Microbiol 15: 1832-1841.
Estelmann, S., Blank, I., Feldmann, A., and Boll, M. (2015) Two distinct old yellow enzymes are involved in naphthyl ring reduction during anaerobic naphthalene degradation. Mol Microbiol 95: 162-172.
Ettwig, K.F., Butler, M.K., Le Paslier, D., Pelletier, E., Mangenot, S., Kuypers, M.M.M. et al. (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464: 543-548.
Galushko, A., Minz, D., Schink, B., and Widdel, F. (1999) Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environ Microbiol 1: 415-420.
Glueck, S.M., Gumus, S., Fabian, W.M.F., and Faber, K. (2010) Biocatalytic carboxylation. Chem Soc Rev 39: 313-328.
Griebler, C., Safinowski, M., Vieth, A., Richnow, H.H., and Meckenstock, R.U. (2004) Combined application of stable carbon isotope analysis and specific metabolites determination for assessing in situ degradation of aromatic hydrocarbons in a tar oil-contaminated aquifer. Environ Sci Technol 38: 617-631.
Gruner, A., Jarling, R., Vieth-Hillebrand, A., Mangelsdorf, K., Janka, C., van der Kraan, G.M., et al. (2017) Tracing microbial hydrocarbon transformation processes in a high temperature petroleum reservoir using signature metabolites. Org Geochem 108: 82-93.
Hahn, C.J., Laso-Pérez, R., Vulcano, F., Vaziourakis, K.M., Stokke, R., Steen, I.H., Teske A., Boetius A., Liebeke M., Amann R., Knittel K., Wegener G. (2020) “Candidatus Ethanoperedens,” a thermophilic genus of archaea mediating the anaerobic oxidation of ethane. MBio 11: e00600-20.
Holler, T., Wegener, G., Niemann, H., Deusner, C., Ferdelman, T.G., Boetius, A., Brunner B., Widdel F. (2011) Carbon and sulfur back flux during anaerobic microbial oxidation of methane and coupled sulfate reduction. Proc Natl Acad Sci USA 108: E1484-E1490.
Kleemann, R., and Meckenstock, R.U. (2011) Anaerobic naphthalene degradation by Gram-positive, iron-reducing bacteria. FEMS Microbiol Ecol 78: 488-496.
Meckenstock, R.U., Annweiler, E., Michaelis, W., Richnow, H.H., and Schink, B. (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66: 2743-2747.
Mihelcic, J.R., and Luthy, R.G. (1988) Microbial-degradation of acenaphthene and naphthalene under denitrification conditions in soil-water systems. Appl Environ Microbiol 54: 1188-1198.
Mouttaki, H., Johannes, J., and Meckenstock, R.U. (2012) Identification of naphthalene carboxylase as a prototype for the anaerobic activation of non-substituted aromatic hydrocarbons. Environ Microbiol 14: 2770-2774.
Musat, F., Galushko, A., Jacob, J., Widdel, F., Kube, M., Reinhardt, R., Wilkes H., Schink B., Rabus R. (2009) Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environ Microbiol 11: 209-219.
Nicholls, D.G., and Ferguson, S.J. (1992) Bioenergetics 2. London: Academic Press.
Nilsen, R.K., Beeder, J., Thorstenson, T., and Torsvik, T. (1996) Distribution of thermophilic marine sulfate reducers in North Sea oil field waters and oil reservoirs. Appl Environ Microbiol 62: 1793-1798.
Orphan, V.J., Taylor, L.T., Hafenbradl, D., and Delong, E.F. (2000) Culture-dependent and culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl Environ Microbiol 66: 700-711.
Poolman, B., and Konings, W.N. (1993) Secondary solute transport in bacteria. BBA-Bioenergetics 1183: 5-39.
Rabus, R., Wilkes, H., Behrends, A., Armstroff, A., Fischer, T., Pierik, A.J., and Widdel, F. (2001) Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: Evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol 183: 1707-1715.
Rockne, K.J., Chee-Sanford, J.C., Sanford, R.A., Hedlund, B.P., Staley, J.T., and Strand, S.E. (2000) Anaerobic naphthalene degradation by microbial pure cultures under nitrate-reducing conditions. Appl Environ Microbiol 66: 1595-1601.
Sebald, W., Machleidt, W., and Wachter, E. (1980) N,N'-dicyclohexylcarbodiimide binds specifically to a single glutamyl residue of the proteolipid subunit of the mitochondrial adenosine-triphosphatases from Neurospora Crassa and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 77: 785-789.
Seewald, J.S. (2003) Organic-inorganic interactions in petroleum-producing sedimentary basins. Nature 426: 327-333.
Sikkema, J., de Bont, J.A., and Poolman, B. (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59: 201-222.
Tissot, B.P., and Welte, D.H. (1984) Petroleum Formation and Occurrence. New York, NY: Springer-Verlag.
Weyrauch, P., Zaytsev, A.V., Stephan, S., Kocks, L., Schmitz, O.J., Golding, B.T., and Meckenstock, R.U. (2017) Conversion of cis-2-carboxycyclohexylacetyl-CoA in the downstream pathway of anaerobic naphthalene degradation. Environ Microbiol 19: 2819-2830.
Widdel, F. (2010) Cultivation of anaerobic microorganisms with hydrocarbons as growth substrates. In Handbook of Hydrocarbon and Lipid Microbiology, Timmis, K. (ed). Springer: Berlin Heidelberg, pp. 3787-3798.
Widdel, F., and Bak, F. (1992) Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes, Balows, A., Trüper, H.G., Dworkin, M., Harder, W., and Schleifer, K.H. (eds). Springer-Verlag New York: New York, NY, pp. 3352-3378.
Widdel, F., and Musat, F. (2010) Energetic and other quantitative aspects of microbial hydrocarbon utilization. In Handbook of Hydrocarbon and Lipid Microbiology, Timmis, K.N. (ed). Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 729-763.
Wise, S.A., Benner, B.A., Byrd, G.D., Chesler, S.N., Rebbert, R.E., and Schantz, M.M. (1988) Determination of polycyclic aromatic-hydrocarbons in a coal-tar standard reference material. Anal Chem 60: 887-894.
Zhang, X.M., and Young, L.Y. (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63: 4759-4764.

Auteurs

Gao Chen (G)

Max Planck Institute for Marine Microbiology, Celsiusstraße 1, Bremen, D-28359, Germany.
Department of Civil and Environmental Engineering, University of Tennessee, Knoxville, TN 37996, USA.

Friedrich Widdel (F)

Max Planck Institute for Marine Microbiology, Celsiusstraße 1, Bremen, D-28359, Germany.

Florin Musat (F)

Max Planck Institute for Marine Microbiology, Celsiusstraße 1, Bremen, D-28359, Germany.
Department of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research - UFZ, Permoserstr., 15, 04318, Leipzig, Germany.

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