The impact of copper, nitrate and carbon status on the emission of nitrous oxide by two species of bacteria with biochemically distinct denitrification pathways

Abstract

SummaryDenitrifying bacteria convert nitrate (NO3 -) to dinitrogen (N2) gas through an anaerobic respiratory process in which the potent greenhouse gas nitrous oxide (N2O) is a free intermediate. These bacteria can be grouped into classes that synthesize a nitrite (NO2 -) reductase (Nir) that is solely dependent on haem-iron as a cofactor (e.g. Paracoccus denitrificans) or a Nir that is solely dependent on copper (Cu) as a cofactor (e.g. Achromobacter xylosoxidans). Regardless of which form of Nir these groups synthesize, they are both dependent on a Cu-containing nitrous oxide reductase (NosZ) for the conversion of N2O to N2. Agriculture makes a major contribution to N2O release and it is recognized that a number of agricultural lands are becoming Cu-limited but are N-rich because of fertilizer addition. Here we utilize continuous cultures to explore the denitrification phenotypes of P. denitrificans and A. xylosoxidans at a range of extracellular NO3

Copper control of bacterial nitrous oxide emission and its impact on vitamin B 12 -dependent metabolism

“…1). These results suggest that in the Cu-L cultures the catalytic capacity of the Cu-dependent Nos system is transiently exceeded by the rate of the reactions that generate nitrous oxide (i.e., NO 3 − , NO 2 − , and NO reduction) and is consistent with other observations that Cu limitation can lead to nitrous oxide release by denitrifying bacteria (7,9,10 This article is a PNAS Direct Submission.…”

“…Expression of the NO 3 − , NO 2 − , NO, and N 2 O reductases are subject to regulation by gas-sensitive regulatory proteins (30), which sense O 2 , NO, or the anion NO 3 − (31-33), and regulate a variety of genes involved in the transition to anaerobic respiration (34). For nearly three decades it has been known that Cu concentrations can drastically affect the activity of N 2 O reductase and the subsequent yield of N 2 O from denitrifying cells (7,9,10). Emerging from this study are two additional features in the biology of this potent green-house gas.…”

“…Under certain conditions, the final step in denitrification is dispensed with and N 2 O is released into the atmosphere. One limiting factor in this process is copper (Cu) availability, the metal cofactor required by the N 2 O reductase (NosZ) that destroys N 2 O (5,7,8). During Cu-limitation the catalytic capacity of the Nos system may be exceeded by the rate of the preceding reactions that generate N 2 O (i.e., NO 3 − , NO 2 − , and NO reduction) and thus, N 2 O is emitted by denitrifying bacteria (7,9,10).…”

“…The possible impact of environmental N 2 O emissions on B 12 metabolism in microbiological communities has largely been ignored. As levels of N 2 O increase in the environment, there is a compelling argument for better understanding the impact of this gaseous intermediate on the regulation of cellular metabolism in denitrifying bacteria, particularly in Cu-limited culture conditions that are associated with N 2 O emissions (7,9). Here we link these two important issues in bacterial N 2 O research and show that the nos genes (for N 2 O reduction) are strongly regulated by Cu and that the accumulation of only micromole amounts of N 2 O in Cu-deficient cultures leads to up-regulation of B 12 independent anabolism, a response indicative of destruction of the B 12 pool by N 2 O.…”

Compaction stimulates denitrification in an urban park soil using 15N tracing technique

“…Numerous studies have examined the factors that influence different pathways involved in denitrification, such as nitrate (Magalhães et al 2005), carbon availability (Henderson et al 2010), pH (Liu et al 2010), and copper concentration (Magalhães et al 2011;Felgate et al 2012). Nevertheless, compaction, as a physical factor, has not received as much attention as the above chemical factors associated with denitrification.…”