Production and consumption of nitrous oxide in nitrate-ammonifying Wolinella succinogenes cells.
Global warming is moving more and more into the public consciousness. Besides the commonly mentioned carbon dioxide and methane, nitrous oxide (N2O) is a powerful greenhouse gas in addition to its contribution to depletion of stratospheric ozone. The increasing concern about N2O emission has focused interest on underlying microbial energy-converting processes and organisms harbouring N2O reductase (NosZ), such as denitrifiers and ammonifiers of nitrate and nitrite. Here, the epsilonproteobacterial model organism Wolinella succinogenes is investigated with regard to its capacity to produce and consume N2O during growth by anaerobic nitrate ammonification. This organism synthesizes an unconventional cytochrome c nitrous oxide reductase (cNosZ), which is encoded by the first gene of an atypical nos gene cluster. However, W. succinogenes lacks a nitric oxide (NO)-producing nitrite reductase of the NirS- or NirK-type as well as an NO reductase of the Nor-type. Using a robotized incubation system, the wild-type strain and suitable mutants of W. succinogenes that either produced or lacked cNosZ were analysed as to their production of NO, N2O and N2 in both nitrate-sufficient and nitrate-limited growth medium using formate as electron donor. It was found that cells growing in nitrate-sufficient medium produced small amounts of N2O, which derived from nitrite and, most likely, from the presence of NO. Furthermore, cells employing cNosZ were able to reduce N2O to N2. This reaction, which was fully inhibited by acetylene, was also observed after adding N2O to the culture headspace. The results indicate that W. succinogenes cells are competent in N2O and N2 production despite being correctly grouped as respiratory nitrate ammonifiers. N2O production is assumed to result from NO detoxification and nitrosative stress defence, while N2O serves as a terminal electron acceptor in anaerobic respiration. The ecological implications of these findings are discussed.
Microbial Energy Conversion and Biotechnology, Department of Biology, Technische Universität Darmstadt, Schnittspahnstraße 10, 64287 Darmstadt, Germany.
Monique
M
Luckmann
Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Chr Falsens vei 1, N1432 Ås, Norway.
Daniel
D
Mania
Microbial Energy Conversion and Biotechnology, Department of Biology, Technische Universität Darmstadt, Schnittspahnstraße 10, 64287 Darmstadt, Germany.
Melanie
M
Kern
Department of Plant and Environmental Sciences, Norwegian University of Life Sciences, PO Box 5003, N1432 Ås, Norway.
Lars R
LR
Bakken
Department of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Chr Falsens vei 1, N1432 Ås, Norway.
Åsa
Å
Frostegård
Microbial Energy Conversion and Biotechnology, Department of Biology, Technische Universität Darmstadt, Schnittspahnstraße 10, 64287 Darmstadt, Germany.
Jörg
J
Simon
D064751:Ammonium Compounds / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D009566:Nitrates / Q000378:metabolism*; D009609:Nitrous Oxide / Q000378:metabolism*; D010088:Oxidoreductases / Q000235:genetics / Q000378:metabolism; D016968:Wolinella / Q000187:drug effects / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*
D064751:Ammonium Compounds; D001426:Bacterial Proteins; D009566:Nitrates; D010088:Oxidoreductases; C022763:nitrous oxide reductase; D009609:Nitrous Oxide