Review PaperFormation of hybrid N2O and hybrid N2 due to codenitrification: First review of a barely considered process of microbially mediated N-nitrosation
Highlights
► Codenitrification is a barely known process of biotic nitrosation. ► It only occurs concomitantly with microbial denitrification. ► The process is proven for archaea, bacteria, and fungi. ► Biotic nitrosation can result in either hybrid N2O/N2 formation or N immobilisation. ► Research on its impact on N cycling within the biosphere is urgently required.
Introduction
The nitrogen (N) cycle is one of the most important nutrient cycles in terrestrial environments and includes four main microbiological processes: N2 fixation, mineralisation, nitrification, and denitrification (Hayatsu et al., 2008). Microbial production of nitrous oxide (N2O) and molecular nitrogen (N2) in the course of N cycling was initially supposed to occur only among particular prokaryotic species either via (i) autotrophic nitrification (e.g., by Nitrosomonas sp.) or by (ii) heterotrophic denitrification (e.g., by Pseudomonas sp.). While the former process was shown to produce N2O during the aerobic oxidation of ammonia (NH3) under limited oxygen (O2) availability (Bremner and Blackmer, 1978, Klemedtsson et al., 1988, Bollmann and Conrad, 1998, Khalil et al., 2004), the latter process was shown to produce both N–N gases (i.e., N2O and N2) during a stepwise anaerobic reduction of nitrate (NO3−) via nitrite (NO2−) and nitric oxide (NO) to N2O and ultimately N2 (Knowles, 1982, Zumft, 1997). However, during recent decades many studies have revealed that microbial N2O and N2 formation within the biosphere is significantly more complex than originally assumed, inasmuch as it exhibits a much broader diversity of microbial species, possible reaction pathways, and range of N compounds utilised (e.g., eukaryotic nitrification and denitrification, heterotrophic nitrification, denitrification by nitrifying species, or anaerobic ammonium (NH4+) oxidation; e.g., Hora and Iyengar, 1960, Bollag and Tung, 1972, Castignetti and Hollocher, 1981, Poth and Focht, 1985, van de Graaf et al., 1990, Shoun et al., 1992, Anderson et al., 1993, Bock et al., 1995, Wrage et al., 2001, Jetten et al., 2005, Müller et al., 2006, Op den Camp et al., 2006, Stange et al., 2009).
Given that our knowledge on microbial N transformations has evolved significantly over the recent decades, Jetten (2008) is correct in stating that even today the microbial world still hides an enormous metabolic capability of N conversion. The intriguing, but less known process of codenitrification appears to perfectly demonstrate his supposition. Codenitrification was first described by Shoun et al. (1992) and Tanimoto et al. (1992) and has been demonstrated to produce N2O and N2 in a different manner compared to nitrification and denitrification. According to these two reports codenitrification refers to a co-metabolic process which utilises N compounds (e.g., NH4+ or amines) differently to the known denitrification pathway (i.e., NO3− → NO2− → NO → N2O → N2) yet converts them to N2O or N2. By means of a 15N tracer technique they revealed that N–N gas production by codenitrification results in a hybrid N–N species, where the N–N bond originates from a combination of an N atom from NO2− and an N atom from a co-metabolised compound. Concomitantly, non-hybrid N–N gas is also formed via the conventional denitrification pathway.
In spite of the unique characteristics found for the codenitrification process (Shoun et al., 1992, Tanimoto et al., 1992) only a few studies have since focused on its elucidation (in particular with respect to microbial N–N gas formation in soils). Most of these were based on cell suspension experiments or were carried out with purified enzymes of denitrifying species (Shoun et al., 1992, Tanimoto et al., 1992, Kumon et al., 2002, Su et al., 2004, Immoos et al., 2004, Shoun, 2004). Only two codenitrification studies have been conducted using soil samples (Laughlin and Stevens, 2002, Spott and Stange, 2011). This is despite the fact that microbial N2O and N2 formation due to codenitrification, as defined in 1992 by Tanimoto et al. and Shoun et al. was obviously already known at about the end of the 19th century.
In 1899 Grimbert reported N gas formation by a denitrifying species, where N gas production significantly exceeded the amount of NO3−–N supplied to a nutrient solution (peptonised broth). It was concluded that the observed surplus of N gas release was caused by amine compounds, which can be utilised in the course of conventional denitrification.
“The evolution of nitrogen is no doubt due to a secondary reaction between the nitrous acid produced by the reduction of the nitrate by the bacillus, and the amino-nitrogen contained in the broth or extract,…” Grimbert (1900)
Half a century later, Allen and van Niel (1952) pointed out that, if an amino group (–NH2) is considered as an additional source of N gas formation during denitrification, then plenty of amines could be considered as possible reactants. Only a few years later Iwasaki et al. (1956) and Iwasaki and Mori (1958) were able to identify some amine species, which in fact caused “excess” N–N gas production when supplied during denitrification. They concluded that in the denitrifying system an N–N-linkage can occur between the amino group of an amine species and an N compound of the denitrification pathway (e.g., NO2−), which then results in the observed “excess” N–N gas production. By means of a 15N tracer technique Garber and Hollocher (1982b) and Kim and Hollocher (1984) confirmed the expected hybrid character of N2O and N2 formed by this reaction. It thus appears that these early reports of hybrid N2O and N2 production are consistent with the definition of codenitrification later on given by Tanimoto et al. (1992) and Shoun et al. (1992). Even in the light of these more recent findings it is intriguing that this apparently significant microbial process has remained almost unconsidered for over a century.
As recently pointed out by Baggs and Philippot (2010) the contribution of codenitrification to soil N2O (and N2) release is still today mostly unknown. In order to close the knowledge gap in the scientific awareness of N–N gas production via codenitrification the present paper reviews (i) the biochemical fundamentals suggested to be responsible for hybrid N2O and hybrid N2 formation during codenitrification, (ii) the microbial species proven or potentially assumed to produce N2O and N2 during codenitrification, and (iii) the N compounds proven to be co-metabolised to N2O and/or N2 via codenitrification. Finally, major environmental controls and the expectable impact of codenitrification on the current picture of N cycling in the biosphere are discussed. The authors cherish the hope that the present review will encourage scientists to focus their research on the study of this intriguing microbial process.
Section snippets
The process of codenitrification
For more than a century studies have reported co-metabolic formation of N2O and/or N2 during conventional denitrification, when particular N compounds (generally amines) are supplied in addition to NO3− (Grimbert, 1899, Renner and Becker, 1970, Kumon et al., 2002), NO2− (Iwasaki et al., 1956, Iwasaki and Mori, 1958, Pichinot et al., 1969, Renner and Becker, 1970, Matsubara, 1970, Garber and Hollocher, 1982b, Kim and Hollocher, 1984, Aerssens et al., 1986, Weeg-Aerssens et al., 1987,
Reports on microbial formation of N2O and N2 by codenitrification
Microbes belonging to bacteria, archaea, and eukarya (kingdom fungi) domains have been reported to act as codenitrifiers or can be at least assumed as codenitrifying species according to the definition of Tanimoto et al. (1992). In total one archaeal species (order Sulfolobales), 12 bacterial species (order Actinomycetales, Burkholderiales, Enterobacteriales, Pseudomonadales, Rhizobiales, and Rhodobacterales), and 3 fungal species (order Hypocreales) have been experimentally demonstrated to
Controlling factors
In principle it can be assumed that the process of codenitrification is controlled by environmental constraints already recognized as controllers of denitrification (see e.g., Knowles, 1982, Zumft, 1997). Hence, an occurrence of codenitrification within the biosphere appears to be mainly controlled by (i) O2 availability, (ii) pH, and (iii) availability of respirable organic carbon substrates. In addition, it can be assumed that codenitrification will be dependent on (iv) the type of
Concluding remarks
Considering N-nitrosation as the fundamental reaction for hybrid N2O and hybrid N2 formation, codenitrification can be viewed as the biotic counterpart of chemical denitrification via N-nitrosation (as e.g., reported by Stevenson and Swaby, 1964, Stevenson et al., 1970, Van Cleemput and Samater, 1996, Thorn and Mikita, 2000, Clough et al., 2001). While during the latter process the nitrosating agent is abiotically formed under acidic conditions via NO2− (e.g., Nelson and Bremner, 1970, Nelson,
Acknowledgements
Our special thanks go to the reviewers for their very helpful annotations and constructive comments. In addition, we would like to thank John Saville Waid for the fantastic support during the peer review process.
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