Abstract
The extended lag period associated with vinyl chloride (VC) starvation in VC- and ethene-assimilating Nocardioides sp. strain JS614 was examined. The extended lag periods were variable (3–7 days), only associated with growth on VC or ethene, and were observed in VC- or ethene-grown cultures following 24 h carbon starvation and mid-exponential phase cultures grown on non-alkene carbon sources (e.g. acetate). Alkene monooxygenase (AkMO) and epoxyalkane:coenzyme M transferase (EaCoMT) are the initial enzymes of VC and ethene biodegradation in strain JS614. Reverse-transcription PCR confirmed that the AkMO gene etnC was expressed in response to epoxyethane, a metabolic intermediate of ethene biodegradation. Epoxyethane (0.5 mM) eliminated the extended lag period in both starved and mid-exponential phase cultures, suggesting that epoxyethane accumulation activates AkMO expression in strain JS614. AkMO activity in ethene-grown cultures was not detected after 6.7 h of carbon starvation, while 40% of the initial EaCoMT activity remained after 24 h. Acetate eliminated the extended lag period in starved cultures but not in mid-exponential phase cultures suggesting that acetate reactivates extant AkMO in starved VC- or ethene-grown cultures. The imbalance between AkMO and EaCoMT activities during starvation likely contributes to the extended lag period by delaying epoxide accumulation and subsequent AkMO induction.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Arenghi FLG, Pinti M, Galli E, Barbieri P (1999) Identification of the Pseudomonas stutzeri OX1 toluene-o-xylene monooxygenase regulatory gene (touR) and of its cognate promoter. Appl Environ Microbiol 65:4057–4063
Bucher JR et al (2001) Ninth Report on carcinogens. In: US Department of Health and Human Services, National Toxicology Program. http://www.ehis.niehs.nih.gov/roc/ninth/known/vinylchloride.pdf
Chen W, Mulchandani A, Deshusses MA (2005) Environmental biotechnology: challenges and opportunities for chemical engineers. AIChE J 51:690–695
Coleman NV, Spain JC (2003) Epoxyalkane:coenzyme M transferase in the ethene and vinyl chloride biodegradation pathways of Mycobacterium strain JS60. J Bacteriol 185:5536–5545
Coleman NV, Mattes TE, Gossett JM, Spain JC (2002a) Biodegradation of cis-dichloroethene as the sole carbon source by a beta-proteobacterium. Appl Environ Microbiol 68:2726–2730
Coleman NV, Mattes TE, Gossett JM, Spain JC (2002b) Phylogenetic and kinetic diversity of aerobic vinyl chloride-assimilating bacteria from contaminated sites. Appl Environ Microbiol 68:6162–6171
Danko AS, Saski CA, Tomkins JP, Freedman DL (2006) Involvement of coenzyme M during aerobic biodegradation of vinyl chloride and ethene by Pseudomonas putida strain AJ and Ochrobactrum sp. strain TD. Appl Environ Microbiol 72:3756–3758
Doughty DM, Sayavedra-Soto LA, Arp DJ, Bottomley PJ (2005) Effects of dichloroethene isomers on the induction and activity of butane monooxygenase in the alkane-oxidizing bacterium “Pseudomonas butanovora”. Appl Environ Microbiol 71:6054–6059
Ensign SA (1996) Aliphatic and chlorinated alkenes and epoxides as inducers of alkene monooxygenase and epoxide activities in Xanthobacter strain Py2. Appl Environ Microbiol 62:61–66
Fathepure BZ, Elango VK, Singh H, Bruner MA (2005) Bioaugmentation potential of a vinyl chloride-assimilating Mycobacterium sp., isolated from a chloroethene-contaminated aquifer. FEMS Microbiol Lett 248:227
Goldberg AL, St John AC (1976) Intracellular protein degradation in mammalian and bacterial cells: part 2. Annu Rev Biochem 45:747–803
de Haan A, Smith MR, Voorhorst WGB, de Bont JA (1993) Co-factor regeneration in the production of 1,2-epoxypropane by Mycobacterium strain E3: the role of storage material. J Gen Microbiol 139:3017–3022
Habets-Crützen AQH, de Bont JAM (1985) Inactivation of alkene oxidation by epoxides in alkene- and alkane-grown bacteria. Appl Microbiol Biotechnol 22:428–433
Hartmans S, de Bont JAM (1992) Aerobic vinyl chloride metabolism in Mycobacterium aurum L1. Appl Environ Microbiol 58:1220–1226
Hartmans S, Weber FJ, Somhorst DPM, de Bont JAM (1991) Alkene monooxygenase from Mycobacterium: a multicomponent enzyme. J Gen Microbiol 137:2555–2560
Kielhorn J, Melber C, Wahnschaffe U, Aitio A, Mangelsdorf I (2000) Vinyl chloride: still a cause for concern. Environ Health Perspect 108:579–588
Krum JG, Ellsworth H, Sargeant RR, Rich G, Ensign SA (2002) Kinetic and microcalorimetric analysis of substrate and cofactor interactions in epoxyalkane:CoM transferase, a zinc-dependent epoxidase. Biochemistry 41:5005–5014
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackbrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 177–203
Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479
Mattes TE, Coleman NV, Gossett JM, Spain JC (2005) Physiological and molecular genetic analyses of vinyl chloride and ethene biodegradation in Nocardioides sp. JS614. Arch Microbiol 183:95–106
Miura A, Dalton H (1995) Purification and characterization of the alkene monooxygenase from Nocardia corallina B-276. Biosci Biotechnol Biochem 59:853–859
Nishino SF, Spain JC (1993) Cell-density dependent adaptation of Pseudomonas putida to biodegradation of p-nitrophenol. Environ Sci Technol 27:489–494
Saeki H, Furuhashi K (1994) Cloning and characterization of a Nocardia corallina B-276 gene cluster encoding alkene monooxygenase. J Ferment Bioeng 78:399–406
Sayavedra-Soto LA, Doughty DM, Kurth EG, Bottomley PJ, Arp DJ (2005) Product and product-independent induction of butane oxidation in Pseudomonas butanovora. FEMS Microbiol Lett 250:111–116
Small FJ, Ensign SA (1997) Alkene monooxygenase from Xanthobacter strain Py2. J Biol Chem 272:24913–24920
Squillace PJ, Moran MJ, Lapham WW, Price CV, Clawges RM, Zogorski JS (1999) Volatile organic compounds in untreated ambient groundwater of the United States, 1985–1995. Environ Sci Technol 33:4176–4187
Stocchi V, Cucchiarini L, Magnani M, Chiarantini L, Palma P, Crescentini G (1985) Simultaneous extraction and reverse-phase high-performance liquid chromatographic determination of adenine and pyridine nucleotides in human red blood cells. Anal Biochem 146:118
Switzer RL (1977) The inactivation of microbial enzymes in vivo. Ann Rev Microbiol 31:135–154
Tropel D, van der Meer JR (2004) Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev 68:474–500
Verce MF, Ulrich RL, Freedman DL (2000) Characterization of an isolate that uses vinyl chloride as a growth substrate under aerobic conditions. Appl Environ Microbiol 66:3535–3542
Weber FJ, van Berkel WJH, Hartmans S, de Bont JAM (1992) Purification and properties of the NADH reductase component of alkene monooxygenase from Mycobacterium strain E3. J Bacteriol 174:3275–3281
Acknowledgments
We thank Juli Rubin, Brian Weisenstein, Linda Rankin, Julie Karceski, and Yang Oh Jin for technical assistance. We also thank Anthony Hay, Ruth Richardson, and Steve Zinder for use of their laboratories and for valuable advice. The U.S. National Science Foundation-supported Center for Environmentally Beneficial Catalysis (NSF award EEC-0310689), the U.S. Strategic Environmental Research and Development Program (SERDP), and The University of Iowa contributed funding for this work.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mattes, T.E., Coleman, N.V., Chuang, A.S. et al. Mechanism controlling the extended lag period associated with vinyl chloride starvation in Nocardioides sp. strain JS614. Arch Microbiol 187, 217–226 (2007). https://doi.org/10.1007/s00203-006-0189-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-006-0189-2