Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis

Luesken FA, Wu ML, den Camp HJMO, Keltjens JT, Stunnenberg H, Francoijs K-J, Strous M, Jetten MSM (2012)
Environmental Microbiology 14(4): 1024-1034.

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Abstract
'Candidatus Methylomirabilis oxyfera' is a denitrifying methanotroph that performs nitrite-dependent anaerobic methane oxidation through a newly discovered intra-aerobic pathway. In this study, we investigated the response of a M. oxyfera enrichment culture to oxygen. Addition of either 2% or 8% oxygen resulted in an instant decrease of methane and nitrite conversion rates. Oxygen exposure also led to a deviation in the nitrite to methane oxidation stoichiometry. Oxygen-uptake and inhibition studies with cell-free extracts displayed a change from cytochrome c to quinol as electron donor after exposure to oxygen. The change in global gene expression was monitored by deep sequencing of cDNA using Illumina technology. After 24 h of oxygen exposure, transcription levels of 1109 (out of 2303) genes changed significantly when compared with the anoxic period. Most of the genes encoding enzymes of the methane oxidation pathway were constitutively expressed. Genes from the denitrification pathway, with exception of one of the putative nitric oxide reductases, norZ2, were severely downregulated. The majority of known genes involved in the vital cellular functions, such as nucleic acid and protein biosynthesis and cell division processes, were downregulated. The alkyl hydroperoxide reductase, ahpC, and genes involved in the synthesis/repair of the iron-sulfur clusters were among the few upregulated genes. Further, transcription of the pmoCAB genes of aerobic methanotrophs present in the non-M. oxyfera community were triggered by the presence of oxygen. Our results show that oxygen-exposed cells of M. oxyfera were under oxidative stress and that in spite of its oxygenic capacity, exposure to microoxic conditions has an overall detrimental effect.
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Luesken FA, Wu ML, den Camp HJMO, et al. Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis. Environmental Microbiology. 2012;14(4):1024-1034.
Luesken, F. A., Wu, M. L., den Camp, H. J. M. O., Keltjens, J. T., Stunnenberg, H., Francoijs, K. - J., Strous, M., et al. (2012). Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis. Environmental Microbiology, 14(4), 1024-1034.
Luesken, F. A., Wu, M. L., den Camp, H. J. M. O., Keltjens, J. T., Stunnenberg, H., Francoijs, K. - J., Strous, M., and Jetten, M. S. M. (2012). Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis. Environmental Microbiology 14, 1024-1034.
Luesken, F.A., et al., 2012. Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis. Environmental Microbiology, 14(4), p 1024-1034.
F.A. Luesken, et al., “Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis”, Environmental Microbiology, vol. 14, 2012, pp. 1024-1034.
Luesken, F.A., Wu, M.L., den Camp, H.J.M.O., Keltjens, J.T., Stunnenberg, H., Francoijs, K.-J., Strous, M., Jetten, M.S.M.: Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis. Environmental Microbiology. 14, 1024-1034 (2012).
Luesken, Francisca A., Wu, Ming L., den Camp, Huub J. M. Op, Keltjens, Jan T., Stunnenberg, Henk, Francoijs, Kees-Jan, Strous, Marc, and Jetten, Mike S. M. “Effect of oxygen on the anaerobic methanotroph 'Candidatus Methylomirabilis oxyfera': kinetic and transcriptional analysis”. Environmental Microbiology 14.4 (2012): 1024-1034.
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Anaerobic oxidation of methane: an "active" microbial process.
Cui M, Ma A, Qi H, Zhuang X, Zhuang G., Microbiologyopen 4(1), 2015
PMID: 25530008
Vertical distribution of nitrite-dependent anaerobic methane-oxidising bacteria in natural freshwater wetland soils.
Shen LD, Huang Q, He ZF, Lian X, Liu S, He YF, Lou LP, Xu XY, Zheng P, Hu BL., Appl. Microbiol. Biotechnol. 99(1), 2015
PMID: 25242345
Biogeographical distribution of denitrifying anaerobic methane oxidizing bacteria in Chinese wetland ecosystems.
Zhu G, Zhou L, Wang Y, Wang S, Guo J, Long XE, Sun X, Jiang B, Hou Q, Jetten MS, Yin C., Environ Microbiol Rep 7(1), 2015
PMID: 25223900
Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake.
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High abundance and diversity of nitrite-dependent anaerobic methane-oxidizing bacteria in a paddy field profile.
Zhou L, Wang Y, Long XE, Guo J, Zhu G., FEMS Microbiol. Lett. 360(1), 2014
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Simultaneous enrichment of denitrifying methanotrophs and anammox bacteria.
Ding ZW, Ding J, Fu L, Zhang F, Zeng RJ., Appl. Microbiol. Biotechnol. 98(24), 2014
PMID: 25056292
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Ecological perspectives on microbes involved in N-cycling.
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Evidence for nitrite-dependent anaerobic methane oxidation as a previously overlooked microbial methane sink in wetlands.
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Rasigraf O, Kool DM, Jetten MS, Sinninghe Damste JS, Ettwig KF., Appl. Environ. Microbiol. 80(8), 2014
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PMID: 23718889
Multiple Rieske/cytb complexes in a single organism.
ten Brink F, Schoepp-Cothenet B, van Lis R, Nitschke W, Baymann F., Biochim. Biophys. Acta 1827(11-12), 2013
PMID: 23507620
Co-localization of particulate methane monooxygenase and cd1 nitrite reductase in the denitrifying methanotroph 'Candidatus Methylomirabilis oxyfera'.
Wu ML, van Alen TA, van Donselaar EG, Strous M, Jetten MS, van Niftrik L., FEMS Microbiol. Lett. 334(1), 2012
PMID: 22681179

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