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Microbial Nitrogen Cycles: Physiology, Genomics and Applications Rick W Ye* and Stuart M Thomas†

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Microbial Nitrogen Cycles: Physiology, Genomics and Applications Rick W Ye* and Stuart M Thomas† 307 Microbial nitrogen cycles: physiology, genomics and applications Rick W Ye* and Stuart M Thomas† G enes and pathways involved in inorganic nitrogen cycles This review summarizes progress made over the past two have been found in traditional as well as unusual years in the understanding of the physiology of microbial microorganisms. These pathways or enzymes play a very metabolism of inorganic nitrogen compounds, and high- important role in the adaptation or survival of these lights the advances made as a result of genome sequencing microorganisms under a variety of environmental conditions. efforts. Additionally, industrial applications of microbial Microbial nitrogen metabolism has industrial applications nitrogen metabolism will be reviewed. ranging from wastewater treatment to bioremediation and potential future use in biocatalysis for chemical production. Dissimilatory reduction of nitrate or nitrite to gaseous forms of nitrogen products Addresses Dissimilatory reduction of nitrate is commonly carried E328/148B, DuPont Experimental Station, Route 141 and out by either a membrane-bound nitrate reductase or a Henry Clay Road, Wilmington, Delaware 19880, USA periplasmic nitrate reductase. The role of these two *e-mail: [email protected] †e-mail: [email protected] types of enzymes in the denitrification process varies, depending on the organism. In the Pseudomonas fluo- Current Opinion in Microbiology 2001, 4:307–312 rescens YT101 strain, only the membrane-bound nitrate 1369-5274/01/$ — see front matter reductase activity is found [6]. Paracoccus pantatropha has © 2001 Elsevier Science Ltd. All rights reserved. both enzymes and the membrane-bound enzyme is responsible for anaerobic denitrification. The periplas- Abbreviations anammox anaerobic ammonia oxidation mic nitrate reductase is suggested to play a role in AOB ammonia-oxidizing bacteria dissipating reductant when this organism is grown on PHA polyhydroxyalkanoates highly reduced carbons under aerobic conditions [7]. For quite a while, the role of periplasmic nitrate reductase in Introduction anaerobic denitrification was uncertain. Recently, it was The metabolism of inorganic nitrogen compounds (see demonstrated that this enzyme is required for anaerobic Figure 1) plays many important physiological roles in nitrate reduction in Pseudomonas sp. G-179 and microorganisms. Denitrification, a process of converting Rhodobacter sphaeroides f. sp. denitrificans [8••,9]. Most nitrate to nitrous oxide or dinitrogen gas, allows nitrate reductases studied so far contain molybdenum in microbes to use alternative electron acceptors to gain the form of a molybdopterin cofactor. Two catalytically energy under oxygen-limiting conditions [1]. distinct, molybdenum-free dissimilatory nitrate reduc- Chemolithotrophic nitrification derives energy from the tases, a soluble periplasmic one and a membrane-bound oxidation of ammonia to nitrite [2]. Dissimilatory reduc- one, were reportedly isolated from the vanadate-reducing tion of nitrate to ammonia under oxygen-limiting bacterium, Pseudomonas isachenkovii [10]. conditions serves as a process to dissipate excess reduc- ing power [3], generates ammonia for assimilation, or There are two types of dissimilatory nitrite reductase supports anaerobic growth with nitrate or nitrite as the that catalyze the conversion of nitrite to nitric oxide in alternative electron acceptors [4]. The newly discovered bacteria. One type is the cytochrome cd1 nitrite reduc- anaerobic ammonia oxidation (anammox) reaction con- tase, and the other type is the copper-containing nitrite verts ammonium and nitrite to dinitrogen gas (see reductase. Based on genome sequencing information, it Figure 2). Although it is not the subject of this review, appears that both types of nitrite reductases are present microbial nitrogen fixation converts gaseous dinitrogen in Methylomonas sp. strain 16a (JM Odom, J-F Tomb, to ammonia for assimilation. In addition, reactions RW Ye, K Norton, A Schenzle, S Zhang, unpublished data). involving inorganic nitrogen species provide a rich variety This observation is the first report of a bacterium that of enzymatic systems for biochemical study [5]. contains both types of dissimilatory nitrite reductases. Detailed biochemical and genetic studies are needed to Microbial nitrogen metabolism also plays an important role validate and elucidate the role of these two enzymes in in the global nitrogen cycle. Microbial activities, such as this organism. The production and consumption of nitric denitrification and anammox, are the major mechanisms oxide have also been reported in other strains of methano- that convert combined nitrogen to dinitrogen gas, thereby trophic bacteria grown in nitrate-containing medium completing the nitrogen cycle. At the same time, microbial under oxygen-limiting conditions [11]. It is likely that activities contribute to the production of greenhouse gases these organisms carry out the assimilatory nitrate reduc- such as nitric and nitrous oxides in the atmosphere. These tion to nitrite, which is then reduced under microbial activities are carried out by a wide variety of micro- oxygen-limiting conditions to nitric oxide and nitrous oganisms that range from archaebacteria to proteobacteria, to oxide via the enzymatic activities of dissimilatory nitrite Gram-positive eubacteria, to fungi. and nitric oxide reductases. 308 Ecology and industrial microbiology Figure 1 Figure 2 + – N2O NH2OH 5H + NO2 N2 Nitrous Hydroxylamine Nitrite Nitrogen NH3 oxide Ammonia Nitrogen Cytoplasm ic fixation Ammonia Electron oxidation transfer y nitr + NH2OH NH4 Biomass Periplasm H+ Membrane- Hydroxylamine Ammonium ion – bound NO2 xide reduction enzyme N2H4 + Nitrite o N2 + 4H Dissimilator Nitrate + Hydrazine Nitrogen NH4 reduction Ammonia ion Current Opinion in Microbiology – – NO NO2 NO3 Nitric oxide Dissimilatory nitrite Nitrite Nitrite Nitrate reduction oxidation Anaerobic ammonium oxidation (anammox) by the Planctomycetales. Anammox is coupled to nitrite reduction. Ammonia and hydroxylamine are Current Opinion in Microbiology converted to hydrazine by a membrane-bound enzyme. Hydrazine is oxidized in the periplasm. The mechanism of electron transfer for nitrite Microbial nitrogen cycle. Nitrate is converted to nitrite by assimilatory reduction is not fully known at this time. Jetten et al. [36] propose two or dissimilatory nitrate reductases. Assimilatory reduction of nitrate to potential systems: one system involves a single enzyme that is responsible ammonia via nitrite enables microbes to use nitrate as the nitrogen for hydrazine oxidation and nitrite reduction, and the other involves a source. Under oxygen-limiting conditions, nitrite can be reduced to nitrite-reducing enzyme that mediates formation of hydroxylamine while an nitric oxide or ammonia. Bacteria with the complete denitrification electron transport chain enzyme supplies the electrons. pathway catalyze the dissimilatory reduction of nitrate to nitrogen. In some bacteria, dissimilatory reduction of nitrate to ammonia via nitrite can support anaerobic growth or dissipate excess reducing power. Ammonia oxidizers oxidize ammonia to hydroxylamine, which is nitrate reduction to ammonia. First of all, B. subtilis was tra- subsequently converted to nitrite. This process also leads to the ditionally believed to be a strict aerobe [4]. It turns out that production of nitric oxide and nitrous oxide. The nitrite produced can B. subtilis can carry out anaerobic dissimilatory reduction of be converted to nitrate by nitrite oxidizers. The nitrification community consists of both ammonia oxidizers and nitrite oxidizers. Anaerobic nitrate to ammonia via nitrite. This anaerobic process has ammonia oxidation (anammox) is shown in Figure 2. long been considered to be a way of dissipating electrons under anaerobic conditions [3]. However, B. subtilis is capa- ble of using nitrate and nitrite as the alternative electron A few types of nitric oxide reductases have been found in acceptors to support anaerobic growth. Anaerobic energy microorganisms. The most common one contains cytochrome generation appears to be coupled to anaerobic fermenta- bc. The cytochrome b nitric oxide reductase lacks the heme c tion, as mutations in lctE and pta (which encode the two subunit [12,13]. The DNA sequence of the cytochrome b enzymes required for lactate and acetate synthesis, respec- enzyme has been found in Neisseria gonorrhoeae [14], Neisseria tively) result in a significant reduction in anaerobic meningitidis [15], Synechocystis sp. PCC6803 [16], Ralstonia fermentative and respiratory growth [20•]. eutrophus [13] and Methylomonas sp. strain 16a (JM Odom, J-F Tomb, RW Ye, K Norton, A Schenzle, S Zhang, unpub- With the availability of the genomic sequence for B. subtilis lished data). This enzyme is required for anaerobic growth of [21], the genome-wide analysis of RNA transcriptional pat- N. gonorrhoeae. In the fungus Fusarium oxysporum, the terns is possible. DNA microarrays, which measure mRNA cytochrome P450 nitric oxide reductase is shown to be levels in a high-throughput manner, have been used to responsible for the step of nitric oxide reduction [17]. In addi- investigate the changes in mRNA transcription when tion, the heme–copper oxidases of Thermus thermophilus and B. subtilis is grown under anaerobic conditions with nitrate cytochrome c nitrite reductase of Sulfurospirillum deleyianum or nitrite as the alternative electron acceptor [22•]. Among can convert nitric oxide to
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