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Diverse electron sources support denitrification under hypoxia in the obligate methanotroph Methylomicrobium album strain BG8.

Kits KD, Campbell DJ, Rosana AR, Stein LY - Front Microbiol (2015)

Bottom Line: Aerobic methane-oxidizing bacteria (MOB) are a diverse group of microorganisms that are ubiquitous in natural environments.Along with anaerobic MOB and archaea, aerobic methanotrophs are critical for attenuating emission of methane to the atmosphere.Our results suggest that expression of denitrification genes, found widely within genomes of aerobic methanotrophs, allow the coupling of substrate oxidation to the reduction of nitrogen oxide terminal electron acceptors under oxygen limitation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Faculty of Science, University of Alberta Edmonton, AB, Canada.

ABSTRACT
Aerobic methane-oxidizing bacteria (MOB) are a diverse group of microorganisms that are ubiquitous in natural environments. Along with anaerobic MOB and archaea, aerobic methanotrophs are critical for attenuating emission of methane to the atmosphere. Clearly, nitrogen availability in the form of ammonium and nitrite have strong effects on methanotrophic activity and their natural community structures. Previous findings show that nitrite amendment inhibits the activity of some cultivated methanotrophs; however, the physiological pathways that allow some strains to transform nitrite, expression of gene inventories, as well as the electron sources that support this activity remain largely uncharacterized. Here we show that Methylomicrobium album strain BG8 utilizes methane, methanol, formaldehyde, formate, ethane, ethanol, and ammonia to support denitrification activity under hypoxia only in the presence of nitrite. We also demonstrate that transcript abundance of putative denitrification genes, nirS and one of two norB genes, increased in response to nitrite. Furthermore, we found that transcript abundance of pxmA, encoding the alpha subunit of a putative copper-containing monooxygenase, increased in response to both nitrite and hypoxia. Our results suggest that expression of denitrification genes, found widely within genomes of aerobic methanotrophs, allow the coupling of substrate oxidation to the reduction of nitrogen oxide terminal electron acceptors under oxygen limitation. The present study expands current knowledge of the metabolic flexibility of methanotrophs by revealing that a diverse array of electron donors support nitrite reduction to nitrous oxide under hypoxia.

No MeSH data available.


Related in: MedlinePlus

Proposed model for NO2- respiration and central metabolism in Methylomicrobium album strain BG8. During hypoxia, M. album strain BG8 utilizes electrons from aerobic CH4 oxidation to respire NO2-. Abbreviations: pMMO, particulate methane monooxygenase; mdh, methanol dehydrogenase; Cyt, cytochrome; nor, nitric oxide reductase; nir, nitrite reductase; ndh, NAD(P)H dehydrogenase complex; Q, coenzyme Q; bc1, cytochrome bc1 complex.
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Figure 6: Proposed model for NO2- respiration and central metabolism in Methylomicrobium album strain BG8. During hypoxia, M. album strain BG8 utilizes electrons from aerobic CH4 oxidation to respire NO2-. Abbreviations: pMMO, particulate methane monooxygenase; mdh, methanol dehydrogenase; Cyt, cytochrome; nor, nitric oxide reductase; nir, nitrite reductase; ndh, NAD(P)H dehydrogenase complex; Q, coenzyme Q; bc1, cytochrome bc1 complex.

Mentions: The present study demonstrates that an aerobic methanotroph – M. album strain BG8 – couples the oxidation of C1 (CH4, CH3OH, CH2O, HCO2H), C2 (C2H6, C2H6O), and inorganic (NH3) substrates to NO2- reduction under O2 limitation resulting in release of the potent greenhouse gas N2O. The ability to couple C1, C2, and inorganic energy sources to O2 respiration and denitrification gives M. album strain BG8 considerable metabolic flexibility. We propose a model for methane driven denitrification in M. album strain BG8 (Figure 6). This discovery has implications for the environmental role of methanotrophic bacteria in the global nitrogen cycle in both N2O emissions and N-loss. Comparing the genome and physiology of the NO2- respiring M. album strain BG8 to NO3- respiring M. denitrificans FJG1 suggests that the inability of M. album strain BG8 to reduce NO3- to N2O is likely due to the absence of a dissimilatory nitrate reductase in the genome, but that expression of predicted denitrification genes, nirS and norB1, enable this aerobic methanotroph to respire NO2-.


Diverse electron sources support denitrification under hypoxia in the obligate methanotroph Methylomicrobium album strain BG8.

Kits KD, Campbell DJ, Rosana AR, Stein LY - Front Microbiol (2015)

Proposed model for NO2- respiration and central metabolism in Methylomicrobium album strain BG8. During hypoxia, M. album strain BG8 utilizes electrons from aerobic CH4 oxidation to respire NO2-. Abbreviations: pMMO, particulate methane monooxygenase; mdh, methanol dehydrogenase; Cyt, cytochrome; nor, nitric oxide reductase; nir, nitrite reductase; ndh, NAD(P)H dehydrogenase complex; Q, coenzyme Q; bc1, cytochrome bc1 complex.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4594100&req=5

Figure 6: Proposed model for NO2- respiration and central metabolism in Methylomicrobium album strain BG8. During hypoxia, M. album strain BG8 utilizes electrons from aerobic CH4 oxidation to respire NO2-. Abbreviations: pMMO, particulate methane monooxygenase; mdh, methanol dehydrogenase; Cyt, cytochrome; nor, nitric oxide reductase; nir, nitrite reductase; ndh, NAD(P)H dehydrogenase complex; Q, coenzyme Q; bc1, cytochrome bc1 complex.
Mentions: The present study demonstrates that an aerobic methanotroph – M. album strain BG8 – couples the oxidation of C1 (CH4, CH3OH, CH2O, HCO2H), C2 (C2H6, C2H6O), and inorganic (NH3) substrates to NO2- reduction under O2 limitation resulting in release of the potent greenhouse gas N2O. The ability to couple C1, C2, and inorganic energy sources to O2 respiration and denitrification gives M. album strain BG8 considerable metabolic flexibility. We propose a model for methane driven denitrification in M. album strain BG8 (Figure 6). This discovery has implications for the environmental role of methanotrophic bacteria in the global nitrogen cycle in both N2O emissions and N-loss. Comparing the genome and physiology of the NO2- respiring M. album strain BG8 to NO3- respiring M. denitrificans FJG1 suggests that the inability of M. album strain BG8 to reduce NO3- to N2O is likely due to the absence of a dissimilatory nitrate reductase in the genome, but that expression of predicted denitrification genes, nirS and norB1, enable this aerobic methanotroph to respire NO2-.

Bottom Line: Aerobic methane-oxidizing bacteria (MOB) are a diverse group of microorganisms that are ubiquitous in natural environments.Along with anaerobic MOB and archaea, aerobic methanotrophs are critical for attenuating emission of methane to the atmosphere.Our results suggest that expression of denitrification genes, found widely within genomes of aerobic methanotrophs, allow the coupling of substrate oxidation to the reduction of nitrogen oxide terminal electron acceptors under oxygen limitation.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Faculty of Science, University of Alberta Edmonton, AB, Canada.

ABSTRACT
Aerobic methane-oxidizing bacteria (MOB) are a diverse group of microorganisms that are ubiquitous in natural environments. Along with anaerobic MOB and archaea, aerobic methanotrophs are critical for attenuating emission of methane to the atmosphere. Clearly, nitrogen availability in the form of ammonium and nitrite have strong effects on methanotrophic activity and their natural community structures. Previous findings show that nitrite amendment inhibits the activity of some cultivated methanotrophs; however, the physiological pathways that allow some strains to transform nitrite, expression of gene inventories, as well as the electron sources that support this activity remain largely uncharacterized. Here we show that Methylomicrobium album strain BG8 utilizes methane, methanol, formaldehyde, formate, ethane, ethanol, and ammonia to support denitrification activity under hypoxia only in the presence of nitrite. We also demonstrate that transcript abundance of putative denitrification genes, nirS and one of two norB genes, increased in response to nitrite. Furthermore, we found that transcript abundance of pxmA, encoding the alpha subunit of a putative copper-containing monooxygenase, increased in response to both nitrite and hypoxia. Our results suggest that expression of denitrification genes, found widely within genomes of aerobic methanotrophs, allow the coupling of substrate oxidation to the reduction of nitrogen oxide terminal electron acceptors under oxygen limitation. The present study expands current knowledge of the metabolic flexibility of methanotrophs by revealing that a diverse array of electron donors support nitrite reduction to nitrous oxide under hypoxia.

No MeSH data available.


Related in: MedlinePlus