Anammox

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A bioreactor containing the anammox bacterium Kuenenia stuttgartiensis Anammox sbr.jpg
A bioreactor containing the anammox bacterium Kuenenia stuttgartiensis

Anammox, an abbreviation for "anaerobic ammonium oxidation", is a globally important microbial process of the nitrogen cycle [1] that takes place in many natural environments. The bacteria mediating this process were identified in 1999, and were a great surprise for the scientific community. [2] In the anammox reaction, nitrite and ammonium ions are converted directly into diatomic nitrogen and water.

Contents

The bacteria that perform the anammox process are genera that belong to the bacterial phylum Planctomycetota. The anammox bacteria all possess one anammoxosome, a lipid bilayer membrane-bound compartment inside the cytoplasm in which the anammox process takes place. [3] [4] The anammoxosome membranes are rich in ladderane lipids; the presence of these lipids is so far unique in biology. [5]

"Anammox" is also the trademarked name for an anammox-based ammonium removal technology developed [6] by the Delft University of Technology.

Process background

C17-C20 ladderane lipids from anammox bacteria containing either three linearly fused cyclobutane rings and one cyclohexane or five cyclobutane rings. Fatty acids are esterified with methanol or the glycerol backbone, and the ladderane alcohols are ether-linked with glycerol, all in different combinations. Ladderane lipids of anammox bacteria.png
C17-C20 ladderane lipids from anammox bacteria containing either three linearly fused cyclobutane rings and one cyclohexane or five cyclobutane rings. Fatty acids are esterified with methanol or the glycerol backbone, and the ladderane alcohols are ether-linked with glycerol, all in different combinations.

In this biological process, which is a redox comproportionation reaction, nitrite and ammonium ions are converted directly into a diatomic molecule of nitrogen and water. [8]

NH+4 + NO−2 → N2 + 2 H2O (ΔG° = −357 kJ⋅mol−1). [9]

Globally, this process may be responsible for 30–50% of the N
2 gas produced in the oceans. [10] It is thus a major sink for fixed nitrogen and so limits oceanic primary productivity.

The bacteria that perform the anammox process belong to the bacterial phylum Planctomycetota. Currently, five anammox genera have been discovered: Brocadia , Kuenenia, Anammoxoglobus, Jettenia (all fresh water species), and Scalindua (marine species). [11] The anammox bacteria are characterized by several striking properties:

The anammox bacteria are geared towards converting their substrates at very low concentrations; in other words, they have a very high affinity to their substrates ammonium and nitrite (sub-micromolar range). [14] [15] Anammox cells are packed with cytochrome c type proteins (≈30% of the protein complement), including the enzymes that perform the key catabolic reactions of the anammox process, making the cells remarkably red. [16] The anammox process was originally found to occur only from 20 °C to 43 °C [14] but more recently, anammox has been observed at temperatures from 36 °C to 52 °C in hot springs [17] and 60 °C to 85 °C at hydrothermal vents located along the Mid-Atlantic Ridge. [18]

History

Figure 2. The biological nitrogen cycle, with dissimilatory nitrate reduction to ammonium The nitrogen cycle Arrigo.png
Figure 2. The biological nitrogen cycle, with dissimilatory nitrate reduction to ammonium

In 1932, it was reported that dinitrogen gas was generated via an unknown mechanism during fermentation in the sediments of Lake Mendota, Wisconsin, USA. [19] In 1965, F. A. Richards [20] noticed that most of the ammonium that should be produced during the anaerobic remineralization of organic matter was unaccounted for. As there was no known biological pathway for this transformation, biological anaerobic oxidation of ammonium received little further attention. [21]

In 1977, Engelbert Broda predicted the existence of two chemolithoautotrophic microorganisms capable of oxidizing ammonium to dinitrogen gas on the basis of thermodynamic calculations. [22] [23] It was thought that anaerobic oxidation of ammonium would not be feasible, assuming that the predecessors had tried and failed to establish a biological basis for those reactions. By the 1990s, Arnold Mulder's observations were just consistent with Richard's suggestion. [24] In their anoxic denitrifying pilot reactor, ammonium disappeared at the expense of nitrite with a clear nitrogen production. The reactor used the effluent from a methanogenic pilot reactor, which contained ammonium, sulphide and other compounds, and nitrate from a nitrifying plant as the influent. The process was named "anammox," and was realized to have great significance in the removal of unwanted ammonium.

The discovery of the anammox process was first publicly presented at the 5th European congress on biotechnology. [25] By the mid-1990s, the discovery of anammox in the fluidized bed reactor was published. [26] A maximum ammonium removal rate of 0.4 kg N/m3/d was achieved. It was shown that for every mole of ammonium consumed, 0.6 mol of nitrate was required, resulting in the formation of 0.8 mol of N
2 gas.

In 1995, the biological nature of anammox was identified. [27] Labeling experiments with 15
NH+
4 in combination with 14
NO−
3 showed that 14-15N
2 was the dominant product making up 98.2% of the total labeled N
2. It was realized that, instead of nitrate, nitrite was assumed as the oxidizing agent of ammonium in anammox reaction. Based on a previous study, Strous et al. [28] calculated the stoichiometry of anammox process by mass balancing, which is widely accepted by other groups. Later, anammox bacteria were identified as Planctomycetota, [2] and the first identified anammox organism was named Candidatus "Brocadia anammoxidans." [29]

Before 2002, anammox was assumed to be a minor player in the nitrogen cycle within natural ecosystems. [30] In 2002 however, anammox was found to play an important part in the biological nitrogen cycle, accounting for 24–67% of the total N
2 production in the continental shelf sediments that were studied. [31] [32] The discovery of anammox process modified the concept of biological nitrogen cycle, as depicted in Figure 2.

Possible reaction mechanisms

Figure 3. Possible biochemical pathway and cellular localization of the enzyme systems involved in anammox reaction. Anammox mechanisms.png
Figure 3. Possible biochemical pathway and cellular localization of the enzyme systems involved in anammox reaction.
Figure 4. Hypothetical metabolic pathways and reversed electron transport in the anammoxosome. (a) Anammox catabolism that uses nitrite as the electron acceptor for the creation of a proton motive force over the anammoxosomal membrane. (b) Proton motive force- driven reversed electron transport combines central catabolism with nitrate reductase (NAR) to generate ferredoxin for carbon dioxide reduction in the acetyl-CoA pathway. HAO, hydrazine oxidoreductase; HD, hydrazine dehydrogenase; HH, hydrazine hydrolase; NIR, nitrite oxidoreductase; Q, quinine. Light blue diamonds, cytochromes; blue arrows, reductions; pink arrows, oxidations. Metabolic pathways.png
Figure 4. Hypothetical metabolic pathways and reversed electron transport in the anammoxosome. (a) Anammox catabolism that uses nitrite as the electron acceptor for the creation of a proton motive force over the anammoxosomal membrane. (b) Proton motive force- driven reversed electron transport combines central catabolism with nitrate reductase (NAR) to generate ferredoxin for carbon dioxide reduction in the acetyl-CoA pathway. HAO, hydrazine oxidoreductase; HD, hydrazine dehydrogenase; HH, hydrazine hydrolase; NIR, nitrite oxidoreductase; Q, quinine. Light blue diamonds, cytochromes; blue arrows, reductions; pink arrows, oxidations.

According to 15
N labeling experiments carried out in 1997, ammonium is biologically oxidized by hydroxylamine, most likely derived from nitrite, as the probable electron acceptor. [33] The conversion of hydrazine to dinitrogen gas is hypothesized to be the reaction that generates the electron equivalents for the reduction of nitrite to hydroxylamine. [34] In general, two possible reaction mechanisms are addressed: [35]

Whether the reduction of nitrite and the oxidation of hydrazine occur at different sites of the same enzyme or the reactions are catalyzed by different enzyme systems connected via an electron transport chain remains to be investigated. [34] In microbial nitrogen metabolism, the occurrence of hydrazine as an intermediate is rare. [36] Hydrazine has been proposed as an enzyme-bound intermediate in the nitrogenase reaction. [37] Recently, using detailed molecular analyses and combining complementary methods, Kartal and coworkers published strong evidence supporting the latter mechanism. [16] [38] Furthermore, the enzyme producing hydrazine, hydrazine synthase was purified and shown to produce hydrazine from NO and ammonium. [16] The production of hydrazine from ammonium and NO was also supported by the resolution of the crystal structure of the enzyme hydrazine synthase. [39]

A possible role of nitric oxide (NO) or nitroxyl (HNO) in anammox was proposed by Hooper et al. [40] by way of condensation of NO or HNO and ammonium on an enzyme related to the ammonium monooxygenase family. The formed hydrazine or imine could subsequently be converted by the enzyme hydroxylamine oxidase to dinitrogen gas, and the reducing equivalents produced in the reaction are required to combine NO or HNO and ammonium or to reduce nitrite to NO. Environmental genomics analysis of the species Candidatus Kuenenia stuttgartiensis , through a slightly different and complementary metabolism mechanism, suggested NO to be the intermediate instead of hydroxylamine (Figure 4). [41] However, this hypothesis also agreed that hydrazine was an important intermediate in the process. In this pathway (Figure 4), there are two enzymes unique to anammox bacteria: hydrazine synthase (hzs) and hydrazine dehydrogenase (hdh). The HZS produces hydrazine from nitric oxide and ammonium, and HDH transfer the electrons from hydrazine to ferredoxin. Few new genes, such as some known fatty acid biosynthesis and S-adenosylmethionine radical enzyme genes, containing domains involved in electron transfer and catalysis have been detected. [41] Anammox microorganisms can also directly couple NO reduction to ammonia oxidation, without the need for nitrite supply. [42]

Another, still unexplored, reaction mechanism involves anaerobic ammonium oxidation on anodes of bio-electrical systems. Such systems can be microbial fuel cells or microbial electrolysis cells. In the absence of dissolved oxygen, nitrite, or nitrate, microbes living in the anode compartment are able to oxidize ammonium to dinitrogen gas (N2) just as in the classical anammox process. [43] At the same time, they unload the liberated electrons onto the anode, producing electrical current. This electrical current can be used either directly in fuel cell mode [44] or for hydrogen and methane gas production in electrolysis mode. [43] While there is no clarity on the reaction mechanism behind, one hypothesis is that nitrite, nitrate, or dinitrogen oxide play a role as intermediates. [44] However, since the process occurs at very low electrochemical potentials, other, more speculative, reaction mechanisms seem possible as well.

Species diversity

Until now, ten anammox species have been described, including seven that are available in laboratory enrichment cultures. [7] All have the taxonomical status of Candidatus , as none were obtained as classical pure cultures. Known species are divided over five genera:

  1. Kuenenia , one species: Kuenenia stuttgartiensis . [41]
  2. Brocadia , three species: B. anammoxidans , B. fulgida , and B. sinica . [2] [45] [46]
  3. Anammoxoglobus , one species: A. propionicus . [47]
  4. Jettenia , one species: J. asiatica . [48] [49]
  5. Scalindua , four species: S. brodae , S. sorokinii , S. wagneri , and S. profunda. [50] [51] [52]

Representatives of the first four genera were enriched from sludge from wastewater treatment plants; K. stuttgartiensis, B. anammoxidans, B. fulgida, and A. propionicus were even obtained from the same inoculum. Scalindua dominates the marine environment, but is also found in some freshwater ecosystems and wastewater treatment plants. [50] [53] [54] [55]

Together, these 10 species likely only represent a minute fraction of anammox biodiversity. For instance, there are currently over 2000 16S rRNA gene sequences affiliated with anammox bacteria that have been deposited to the Genbank (https://www.ncbi.nlm.nih.gov/genbank/), representing an overlooked continuum of species, subspecies, and strains, each apparently having found its specific niche in the wide variety of habitats where anammox bacteria are encountered. Species microdiversity is particularly impressive for the marine representative Scalindua. [51] [56] [57] [58] [59] [60] A question that remains to be investigated is which environmental factors determine species differentiation among anammox bacteria.

The sequence identities of the anammox 16S rRNA genes range from 87 to 99%, and phylogenetic analysis places them all within the phylum Planctomycetota, [61] which form the PVC superphylum together with Verrucomicrobia and Chlamydiae. [62] Within the Planctomycetota, anammox bacteria deeply branch as a monophyletic clade. Their phylogenetic position together with a broad range of specific physiological, cellular, and molecular traits give anammox bacteria their own order Brocadiales. [63]

Application in wastewater treatment

The application of the anammox process lies in the removal of ammonium in the wastewater treatment and consists of two separate processes.
The first step is the partial nitrification (nitritation) of half of the ammonium to nitrite by ammonia oxidizing bacteria:

2 NH+
4 + 3 O
2 → 2 NO−
2 + 4 H+
 + 2 H
2O

The remaining half of the ammonium and the newly formed nitrite are converted in the anammox process to diatomic nitrogen gas and ~15 % nitrate (not shown) by anammox bacteria:

NH+
4 + NO−
2 → N
2 + 2 H
2O

Both processes can take place in 1 reactor where two guilds of bacteria form compact granules. [64] [65]

For the enrichment of the anammox organisms a granular biomass or biofilm system seems to be especially suited in which the necessary sludge age of more than 20 days can be ensured. Possible reactors are sequencing batch reactors (SBR), moving bed reactors or gas-lift-loop reactors. The cost reduction compared to conventional nitrogen removal is considerable; the technique is still young but proven in several fullscale installations. [66]

The first full scale reactor intended for the application of anammox bacteria was built in the Netherlands in 2002. [67] In other wastewater treatment plants, such as the one in Germany (Hattingen), anammox activity is coincidentally observed though were not built for that purpose. As of 2006, there are three full scale processes in The Netherlands: one in a municipal wastewater treatment plant (in Rotterdam), and two on industrial effluent. One is a tannery, the other a potato processing plant. [68]

Advantages

Conventional nitrogen removal from ammonium-rich wastewater is accomplished in two separate steps: nitrification, which is mediated by aerobic ammonia- and nitrite-oxidizing bacteria and denitrification carried out by denitrifiers, which reduce nitrate to N
2 with the input of suitable electron donors. Aeration and input of organic substrates (typically methanol) show that these two processes are: [69]

  1. Highly energy consuming.
  2. Associated with the production of excess sludge.
  3. Produce significant amounts of green-house gases such as CO2 and N
    2    O     and ozone-depleting NO.

Because anammox bacteria convert ammonium and nitrite directly to N
2 anaerobically, this process does not require aeration and other electron donors. Nevertheless, oxygen is still required for the production of nitrite by ammonia-oxidizing bacteria. However, in partial nitritation/anammox systems, oxygen demand is greatly reduced because only half of the ammonium needs to be oxidized to nitrite instead of full conversion to nitrate. The autotrophic nature of anammox bacteria and ammonia-oxidizing bacteria guarantee a low yield and thus less sludge production. [69] Additionally, anammox bacteria easily form stable self-aggregated biofilm (granules) allowing reliable operation of compact systems characterized by high biomass concentration and conversion rate up to 5–10 kg N m−3. [70] Overall, it has been shown that efficient application of the anammox process in wastewater treatment results in a cost reduction of up to 60% [71] [72] as well as lower CO2 emissions. [69]

Disadvantages

The doubling time is slow, between 10 days to 2 weeks. [73] This makes it difficult to grow enough sludge for a wastewater treatment reactor. Also the recovery time after the loss of sludge by accident is longer than in conventional nitrogen removal systems. On the other hand, this slow growing rate is an advantage due to the reduction of surplus sludge that needs to be removed and treated. Depending on the exact species, the optimum pH level is 8. [73] Therefore, it can be necessary to adjust the pH of the wastewater by adding caustic.

Related Research Articles

<span class="mw-page-title-main">Denitrification</span> Microbially facilitated process

Denitrification is a microbially facilitated process where nitrate (NO3−) is reduced and ultimately produces molecular nitrogen (N2) through a series of intermediate gaseous nitrogen oxide products. Facultative anaerobic bacteria perform denitrification as a type of respiration that reduces oxidized forms of nitrogen in response to the oxidation of an electron donor such as organic matter. The preferred nitrogen electron acceptors in order of most to least thermodynamically favorable include nitrate (NO3−), nitrite (NO2−), nitric oxide (NO), nitrous oxide (N2O) finally resulting in the production of dinitrogen (N2) completing the nitrogen cycle. Denitrifying microbes require a very low oxygen concentration of less than 10%, as well as organic C for energy. Since denitrification can remove NO3−, reducing its leaching to groundwater, it can be strategically used to treat sewage or animal residues of high nitrogen content. Denitrification can leak N2O, which is an ozone-depleting substance and a greenhouse gas that can have a considerable influence on global warming.

Methanotrophs are prokaryotes that metabolize methane as their source of carbon and chemical energy. They are bacteria or archaea, can grow aerobically or anaerobically, and require single-carbon compounds to survive.

<i>Candidatus</i> Brocadia anammoxidans Species of bacterium

"Candidatus Brocadia anammoxidans" is a bacterial member of the phylum Planctomycetota and therefore lacks peptidoglycan in its cell wall, and has a compartmentalized cytoplasm.

Denitrifying bacteria are a diverse group of bacteria that encompass many different phyla. This group of bacteria, together with denitrifying fungi and archaea, is capable of performing denitrification as part of the nitrogen cycle. Denitrification is performed by a variety of denitrifying bacteria that are widely distributed in soils and sediments and that use oxidized nitrogen compounds such as nitrate and nitrite in the absence of oxygen as a terminal electron acceptor. They metabolize nitrogenous compounds using various enzymes, including nitrate reductase (NAR), nitrite reductase (NIR), nitric oxide reductase (NOR) and nitrous oxide reductase (NOS), turning nitrogen oxides back to nitrogen gas or nitrous oxide.

Microbial metabolism is the means by which a microbe obtains the energy and nutrients it needs to live and reproduce. Microbes use many different types of metabolic strategies and species can often be differentiated from each other based on metabolic characteristics. The specific metabolic properties of a microbe are the major factors in determining that microbe's ecological niche, and often allow for that microbe to be useful in industrial processes or responsible for biogeochemical cycles.

<span class="mw-page-title-main">Sequencing batch reactor</span> Type of activated sludge process for the treatment of wastewater

Sequencing batch reactors (SBR) or sequential batch reactors are a type of activated sludge process for the treatment of wastewater. SBRs treat wastewater such as sewage or output from anaerobic digesters or mechanical biological treatment facilities in batches. Oxygen is bubbled through the mixture of wastewater and activated sludge to reduce the organic matter. The treated effluent may be suitable for discharge to surface waters or possibly for use on land.

Nitrifying bacteria are chemolithotrophic organisms that include species of genera such as Nitrosomonas, Nitrosococcus, Nitrobacter, Nitrospina, Nitrospira and Nitrococcus. These bacteria get their energy from the oxidation of inorganic nitrogen compounds. Types include ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB). Many species of nitrifying bacteria have complex internal membrane systems that are the location for key enzymes in nitrification: ammonia monooxygenase, hydroxylamine oxidoreductase, and nitrite oxidoreductase.

<span class="mw-page-title-main">Ladderane</span>

In chemistry, a ladderane is an organic molecule containing two or more fused cyclobutane rings. The name arises from the resemblance of a series of fused cyclobutane rings to a ladder. Numerous synthetic approaches have been developed for the synthesis of ladderane compounds of various lengths. The mechanisms often involve [2 + 2] photocycloadditions, a useful reaction for creating strained 4-membered rings. Naturally occurring ladderanes have been identified as major components of the anammoxosome membrane of the anammox bacteria, phylum Planctomycetota.

Anaerobic oxidation of methane (AOM) is a methane-consuming microbial process occurring in anoxic marine and freshwater sediments. AOM is known to occur among mesophiles, but also in psychrophiles, thermophiles, halophiles, acidophiles, and alkophiles. During AOM, methane is oxidized with different terminal electron acceptors such as sulfate, nitrate, nitrite and metals, either alone or in syntrophy with a partner organism.

CandidatusScalindua wagneri is a Gram-negative coccoid-shaped bacterium that was first isolated from a wastewater treatment plant. This bacterium is an obligate anaerobic chemolithotroph that undergoes anaerobic ammonium oxidation (anammox). It can be used in the wastewater treatment industry in nitrogen reactors to remove nitrogenous wastes from wastewater without contributing to fixed nitrogen loss and greenhouse gas emission.

"Candidatus Scalindua" is a bacterial genus, and a proposed member of the order Planctomycetales. These bacteria lack peptidoglycan in their cell wall and have a compartmentalized cytoplasm. They are ammonium oxidizing bacteria found in marine environments.

Hydrazine oxidoreductase (EC 1.7.99.8, HAO (ambiguous)) is an enzyme with systematic name hydrazine:acceptor oxidoreductase. This enzyme catalyses the following chemical reaction

Candidatus Brocadia fulgida is a prokaryotic species of bacteria that performs the anammox process. Fatty acids constitute an enrichment culture for B. fulgida. The species' 16S ribosomal RNA sequence has been determined. During the anammox process, it oxidizes acetate at the highest rate and outcompetes other anammox bacteria, which indicates that it does not incorporate acetate directly into its biomass like other anammox bacteria.

Comammox is the name attributed to an organism that can convert ammonia into nitrite and then into nitrate through the process of nitrification. Nitrification has traditionally thought to be a two-step process, where ammonia-oxidizing bacteria and archaea oxidize ammonia to nitrite and then nitrite-oxidizing bacteria convert to nitrate. Complete conversion of ammonia into nitrate by a single microorganism was first predicted in 2006. In 2015 the presence of microorganisms that could carry out both conversion processes was discovered within the genus Nitrospira, and the nitrogen cycle was updated. Within the genus Nitrospira, the major ecosystems comammox are primarily found in natural aquifers and engineered ecosystems.

Dissimilatory nitrate reduction to ammonium (DNRA), also known as nitrate/nitrite ammonification, is the result of anaerobic respiration by chemoorganoheterotrophic microbes using nitrate (NO3−) as an electron acceptor for respiration. In anaerobic conditions microbes which undertake DNRA oxidise organic matter and use nitrate (rather than oxygen) as an electron acceptor, reducing it to nitrite, and then to ammonium (NO3− → NO2− → NH4+).

<span class="mw-page-title-main">NC10 phylum</span> Phylum of bacteria

NC10 is a bacterial phylum with candidate status, meaning its members remain uncultured to date. The difficulty in producing lab cultures may be linked to low growth rates and other limiting growth factors.

CandidatusAnammoxoglobus propionicus is an anammox bacteria that is taxonomically in the phylum of Planctomycetota. Anammoxoglobus propionicus is an interest to many researchers due to its ability to reduce nitrite and oxidize ammonium into nitrogen gas and water.

<i>Methylomirabilis oxyfera</i> Bacteria species

Candidatus "Methylomirabilis oxyfera" is a candidate species of Gram-negative bacteria belonging to the NC10 phylum, characterized for its capacity to couple anaerobic methane oxidation with nitrite reduction in anoxic environments. To acquire oxygen for methane oxidation, M. oxyfera utilizes an intra-aerobic pathway through the reduction of nitrite (NO2) to dinitrogen (N2) and oxygen.

"Candidatus Brocadia" is a candidatus genus of bacteria, meaning that while it is well-characterized, it has not been grown as a pure culture yet. Due to this, much of what is known about Candidatus species has been discovered using culture-independent techniques such as metagenomic sequence analysis.

Anammox is a wastewater treatment technique that removes nitrogen using anaerobic ammonium oxidation (anammox). This process is performed by anammox bacteria which are autotrophic, meaning they do not need organic carbon for their metabolism to function. Instead, the metabolism of anammox bacteria convert ammonium and nitrite into dinitrogen gas. Anammox bacteria are a wastewater treatment technique and wastewater treatment facilities are in the process of implementing anammox-based technologies to further enhance ammonia and nitrogen removal.

References

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