Nitrosopumilus

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Nitrosopumilus
ThaspiviridaeFig1rv2.png
Nitrosopumilus maritimus, partially with virions of Nitrosopumilus spindle-shaped virus 1 ( Thaspiviridae ) attached.
Scientific classification
Domain:
Phylum:
Class:
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Genus:
Nitrosopumilus

Qin et al. 2017
Type species
Nitrosopumilus maritimus
Qin et al. 2017
Species
Synonyms
  • "Ca. Nitrosopumilus" Konneke et al. 2005
  • "Ca. Nitrosomarinus" Ahlgren et al. 2017

Nitrosopumilus maritimus is an extremely common archaeon living in seawater. It is the first member of the Group 1a Nitrososphaerota (formerly Thaumarchaeota) to be isolated in pure culture. Gene sequences suggest that the Group 1a Nitrososphaerota are ubiquitous with the oligotrophic surface ocean and can be found in most non-coastal marine waters around the planet. [1] It is one of the smallest living organisms at 0.2 micrometers in diameter. Cells in the species N. maritimus are shaped like peanuts and can be found both as individuals and in loose aggregates. [2] They oxidize ammonia to nitrite and members of N. maritimus can oxidize ammonia at levels as low as 10 nanomolar, near the limit to sustain its life. [3] Archaea in the species N. maritimus live in oxygen-depleted habitats. Oxygen needed for ammonia oxidation might be produced by novel pathway which generates oxygen and dinitrogen. [4] N. maritimus is thus among organisms which are able to produce oxygen in dark.

Contents

This organism was isolated from sediment in a tropical tank at the Seattle Aquarium by a group led by David Stahl (University of Washington). [5]

Biology

Lipid membranes

Populations of N. maritimus are probably the main source of glycerol dialkyl glycerol tetraethers (GDGTs) in the ocean, a compound which constitutes their monolayer lipidic cell membranes as intact polar lipids (IPLs) [6] together with crenarcheol. [7] This membrane structure is thought to maximise proton motive force. [6] The compounds found in the membrane of these organisms, such as GDGTs, IPLs, and crenarcheol, can be useful as biomarkers for the presence of organisms belonging to the Nitrososphaerota group in the water column. [6]   These archaea have also been found to change their membrane's composition in relation to temperature (by GDGT cyclization), growth, [8] metabolic status, [9] and, even if less dramatically, to pH. [6]

Cell division

Euryarchaeota, Thermoproteota, and Nitrososphaerota are some of the three major phyla of Archaea which use cell division to duplicate. Euryarchaeota and Bacteria use the FtsZ mechanism in cell division, while Thermoproteota divide using the Cdv machinery. However, Nitrososphaerota such as N. maritimus adopts both mechanisms, FtsZ and Cdv. Nevertheless, after further researches, N. maritimus was found to use mainly Cdv proteins rather than FtsZ during cell division. In this case, Cdv is the primary system in cell division for N. maritimus. [10] [11] Therefore, to replicate a genome of 1.645Mb, N. maritimus spends 15 to 18 hours. [12]

Physiology

Genome

Ammonia-oxidizing bacteria (AOB) are known to have chemolithoautotrophic growth by using inorganic carbon, N. maritimus, an Ammonia-oxidizing archaea (AOA) use a similar process of growth. While AOB uses Calvin–Bassham–Benson cycle with the CO2-fixing enzyme ribulose bisphosphate carboxylase/oxygenase (RubisCO) as the key enzyme; N. maritimus seems to grow and use an alternative pathway due to the lack of genes and enzymes. Therefore, a variant of the 3-hydroxypropionate/4-hydroxybutyrate is used by N. maritimus to develop autotrophically, which allows its capacity to assimilate inorganic carbon. [13] Using the 3-hydroxypropionate/4-hydroxybutyrate pathway method instead of the Calvin cycle, N. maritimus could provide a growth advantage as the process is more energy-efficient. Due to its originality, N. maritimus plays an essential role in the carbon and nitrogen cycle [14]

Ammonia Oxidizing

The isolation and the sequencing of N. maritimus's genome have allowed to extend the insight into the physiology of the organisms belonging to the Nitrososphaerota group. N. maritimus was the first Archaeon with an ammonia oxidizing metabolism to be studied. This organism is common in the marine environment especially at the bottom of the photic zone where the amount of Ammonium and Iron is enough to support its growth. [15] The physiology of N. maritimus remains unclear under certain aspects. It conserves energy for its vital functions, from the oxidation of Ammonia and the reduction of Oxygen, with the formation of Nitrite. CO2 is the carbon source. It is fixed and assimilated by the microorganism through the 3-hydroxypropinate/4-hydroxybutyrate carbon cycle. [16] N. maritimus carries out the first step of Nitrification, by acting in a key role in the Nitrogen cycle along the water column. Since this oxidizing reaction releases just a little amount of energy, the growth of this microorganism is slow. N. maritimus’s genome includes the amoA gene, encoding for the Ammonia Monooxygenase (AMO) enzyme. This latter allows the oxidation of ammonia to hydroxylamine (NH2OH). Instead, the genome lacks the gene encoding for Hydroxylamine Oxidoreductase (HAO) responsible for oxidizing the intermediate (NH2OH) to nitrite. The hydroxylamine is produced as a metabolite, and it is immediately consumed during the metabolic reaction. Other intermediates produced during this metabolic pathway are: the nitric oxide (NO), the nitrous oxide (N2O), the nitoxyl (HNO). These are toxic at high concentration. The enzyme responsible for oxidizing the hydroxylamine to nitrite is not well-known yet. [17] Two hypotheses are suggested for the metabolic pathway of N. maritimus that involve two types of enzymes  : the copper-based enzyme (Cu-ME) and the nitrite reductase enzyme (nirK) and its reverse: [18]

•In the first one ammonia is oxidized through AMO forming the hydroxylamine; the latter, plus a molecule of nitric oxide, are, in turn, oxidized by a copper-based enzyme (Cu-ME) producing two molecules of nitrite. One of these is reduced to NO by the nitrite reductase (nirK) and goes back to the cu-ME enzyme. An electrons translocation occurs producing a Proton Motive Force (PMF) and allowing ATP synthesis.

•In the second one ammonia is oxidized through AMO making up the Hydroxylamine and then the two enzymes, nirK and Cu-ME, oxidize the hydroxylamine to nitric oxide and this to nitrite. The proper roles and the order at which these enzymes work, have to be clarified.

Additionally nitrous oxide is released by this type of metabolism. It is an important greenhouse gas that likely is produced as result of abiotic denitrification of metabolites.

Taxonomy

The currently accepted taxonomy is based on the List of Prokaryotic names with Standing in Nomenclature (LPSN) [19] and National Center for Biotechnology Information (NCBI) [20]

16S rRNA based LTP_06_2022 [21] [22] [23] 53 marker proteins based GTDB 08-RS214 [24] [25] [26]
Nitrosopumilus

N. zosterae

"N. ureiphilus"

N. adriaticus

N. maritimus

N. piranensis

"N. cobalaminigenes"

"N. oxyclinae"

Nitrosopumilus

N. maritimus Qin et al. 2017

"Ca. N. koreensis" Park et al. 2012

N. piranensisBayer et al. 2019

N. zosteraeNakagawa et al. 2021

N. adriaticusBayer et al. 2019

"N. ureiphilus" Qin et al. 2017

"Ca. N. salarius" corrig. Mosier et al. 2012

"Ca. N. catalinensis" (Ahlgren et al. 2017) Rinke et al. 2020

"Ca. N. limneticus" Klotz et al. 2022

"Ca. N. sediminis" Park et al. 2012

"N. cobalaminigenes" Qin et al. 2017

"N. oxyclinae" Qin et al. 2017

Ecology

Habitats

Characteristic of the Nitrososphaerota phylum, N. maritimus [27] is mainly found in oligotrophic (poor environment in nutrients) open ocean, within the Pelagic zone. [28] Initially discovered in Seattle, in an aquarium, [29] today N. maritimus can populate numerous environment such as the subtropical North Pacific and South Atlantic Ocean or the mesopelagic zone in the Pacific Ocean. [30] N. maritimus is an aerobic archeon able to grow even with an extremely low concentration of nutrients, [31] like in dark-deep open ocean, in which N. maritimus as an important impact. [32]

Contributions

Nitrification of the ocean

Members of the species N. maritimus can oxidize ammonia to form nitrite, which is the first step of the nitrogen cycle. Ammonia and nitrate are the two nutrients which form the inorganic pool of nitrogen. Populating poor environments (lacking of organic energy sources and sunlight), the oxidation of ammonia could contribute to primary productivity . [29] In fact, nitrate fuels half of the primary production of phytoplankton [33] but not only phytoplankton needs nitrate. The high ammonia's affinity allows N. maritimus to largely compete with the other marine phototrophs and chemotrophs. [31] Regarding the ammonium turnover per unit biomass, N. maritimus would be around 5 times higher than oligotrophic heterotrophs' turnover, and around 30 times higher than most of the oligotrophic diatoms known turnover. [31] Computing these two observations nitrification by N. maritimus plays a key role in the marine nitrogen cycle. [34]

Carbon and phosphorus implications

Its ability to fix inorganic carbon via an alternative pathway (3-hydroxypropionate/4-hydroxybutyrate pathway) [28] allows N. maritimus to participate efficiently in the flux of the global carbon budget. [32] Coupling with the ammonia-oxidizing pathway, N. maritimus and the other marine thaumarchaea, approximately, recycle 4.5% of the organic carbon mineralized in the oceans and transform 4.3% of detrital phosphorus into new phosphorus substances. [32]

See also

Related Research Articles

<span class="mw-page-title-main">Nitrification</span> Biological oxidation of ammonia/ammonium to nitrate

Nitrification is the biological oxidation of ammonia to nitrate via the intermediary nitrite. Nitrification is an important step in the nitrogen cycle in soil. The process of complete nitrification may occur through separate organisms or entirely within one organism, as in comammox bacteria. The transformation of ammonia to nitrite is usually the rate limiting step of nitrification. Nitrification is an aerobic process performed by small groups of autotrophic bacteria and archaea.

<span class="mw-page-title-main">Anammox</span> Anaerobic ammonium oxidation, a microbial process of the nitrogen cycle

Anammox, an abbreviation for "anaerobic ammonium oxidation", is a globally important microbial process of the nitrogen cycle 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. In the anammox reaction, nitrite and ammonium ions are converted directly into diatomic nitrogen and water.

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>Nitrosomonas</i> Genus of bacteria

Nitrosomonas is a genus of Gram-negative bacteria, belonging to the Betaproteobacteria. It is one of the five genera of ammonia-oxidizing bacteria and, as an obligate chemolithoautotroph, uses ammonia as an energy source and carbon dioxide as a carbon source in presence of oxygen. Nitrosomonas are important in the global biogeochemical nitrogen cycle, since they increase the bioavailability of nitrogen to plants and in the denitrification, which is important for the release of nitrous oxide, a powerful greenhouse gas. This microbe is photophobic, and usually generate a biofilm matrix, or form clumps with other microbes, to avoid light. Nitrosomonas can be divided into six lineages: the first one includes the species Nitrosomonas europea, Nitrosomonas eutropha, Nitrosomonas halophila, and Nitrosomonas mobilis. The second lineage presents the species Nitrosomonas communis, N. sp. I and N. sp. II, meanwhile the third lineage includes only Nitrosomonas nitrosa. The fourth lineage includes the species Nitrosomonas ureae and Nitrosomonas oligotropha and the fifth and sixth lineages include the species Nitrosomonas marina, N. sp. III, Nitrosomonas estuarii and Nitrosomonas cryotolerans.

<i>Nitrobacter</i> Genus of bacteria

Nitrobacter is a genus comprising rod-shaped, gram-negative, and chemoautotrophic bacteria. The name Nitrobacter derives from the Latin neuter gender noun nitrum, nitri, alkalis; the Ancient Greek noun βακτηρία, βακτηρίᾱς, rod. They are non-motile and reproduce via budding or binary fission. Nitrobacter cells are obligate aerobes and have a doubling time of about 13 hours.

Methanosarcina acetivorans is a versatile methane producing microbe which is found in such diverse environments as oil wells, trash dumps, deep-sea hydrothermal vents, and oxygen-depleted sediments beneath kelp beds. Only M. acetivorans and microbes in the genus Methanosarcina use all three known metabolic pathways for methanogenesis. Methanosarcinides, including M. acetivorans, are also the only archaea capable of forming multicellular colonies, and even show cellular differentiation. The genome of M. acetivorans is one of the largest archaeal genomes ever sequenced. Furthermore, one strain of M. acetivorans, M. a. C2A, has been identified to possess an F-type ATPase along with an A-type ATPase.

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.

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.

Nitrospira translate into “a nitrate spiral” is a genus of bacteria within the monophyletic clade of the Nitrospirota phylum. The first member of this genus was described 1986 by Watson et al. isolated from the Gulf of Maine. The bacterium was named Nitrospira marina. Populations were initially thought to be limited to marine ecosystems, but it was later discovered to be well-suited for numerous habitats, including activated sludge of wastewater treatment systems, natural biological marine settings, water circulation biofilters in aquarium tanks, terrestrial systems, fresh and salt water ecosystems, and hot springs. Nitrospira is a ubiquitous bacterium that plays a role in the nitrogen cycle by performing nitrite oxidation in the second step of nitrification. Nitrospira live in a wide array of environments including but not limited to, drinking water systems, waste treatment plants, rice paddies, forest soils, geothermal springs, and sponge tissue. Despite being abundant in many natural and engineered ecosystems Nitrospira are difficult to culture, so most knowledge of them is from molecular and genomic data. However, due to their difficulty to be cultivated in laboratory settings, the entire genome was only sequenced in one species, Nitrospira defluvii. In addition, Nitrospira bacteria's 16S rRNA sequences are too dissimilar to use for PCR primers, thus some members go unnoticed. In addition, members of Nitrospira with the capabilities to perform complete nitrification has also been discovered and cultivated.

<span class="mw-page-title-main">Cenarchaeum</span> Genus of archaea

In taxonomy, Cenarchaeum is a genus of the Cenarchaeaceae. The marine archaean Cenarchaeum symbiosum lives within the sponge Axinella mexicana.

Nitrite oxidoreductase is an enzyme involved in nitrification. It is the last step in the process of aerobic ammonia oxidation, which is carried out by two groups of nitrifying bacteria: ammonia oxidizers such as Nitrosospira, Nitrosomonas, and Nitrosococcus convert ammonia to nitrite, while nitrite oxidizers such as Nitrobacter and Nitrospira oxidize nitrite to nitrate. NXR is responsible for producing almost all nitrate found in nature.

Hydroxylamine oxidoreductase (HAO) is an enzyme found in the prokaryotic genus Nitrosomonas. It plays a critically important role in the biogeochemical nitrogen cycle as part of the metabolism of ammonia-oxidizing bacteria.

<span class="mw-page-title-main">Archaea</span> Domain of single-celled organisms

Archaea is a domain of single-celled organisms. These microorganisms lack cell nuclei and are therefore prokaryotes. Archaea were initially classified as bacteria, receiving the name archaebacteria, but this term has fallen out of use.

<span class="mw-page-title-main">Nitrososphaerota</span> Phylum of archaea

The Nitrososphaerota are a phylum of the Archaea proposed in 2008 after the genome of Cenarchaeum symbiosum was sequenced and found to differ significantly from other members of the hyperthermophilic phylum Thermoproteota. Three described species in addition to C. symbiosum are Nitrosopumilus maritimus, Nitrososphaera viennensis, and Nitrososphaera gargensis. The phylum was proposed in 2008 based on phylogenetic data, such as the sequences of these organisms' ribosomal RNA genes, and the presence of a form of type I topoisomerase that was previously thought to be unique to the eukaryotes. This assignment was confirmed by further analysis published in 2010 that examined the genomes of the ammonia-oxidizing archaea Nitrosopumilus maritimus and Nitrososphaera gargensis, concluding that these species form a distinct lineage that includes Cenarchaeum symbiosum. The lipid crenarchaeol has been found only in Nitrososphaerota, making it a potential biomarker for the phylum. Most organisms of this lineage thus far identified are chemolithoautotrophic ammonia-oxidizers and may play important roles in biogeochemical cycles, such as the nitrogen cycle and the carbon cycle. Metagenomic sequencing indicates that they constitute ~1% of the sea surface metagenome across many sites.

Ammonia monooxygenase (EC 1.14.99.39, AMO) is an enzyme, which catalyses the following chemical reaction

Nitrososphaera is a mesophilic genus of ammonia-oxidizing Crenarchaeota. The first Nitrososphaera organism was discovered in garden soils at the University of Vienna leading to the categorization of a new genus, family, order and class of Archaea. This genus is contains three distinct species: N. viennensis, Ca. N. gargensis, and Ca N. evergladensis. Nitrososphaera are chemolithoautotrophs and have important biogeochemical roles as nitrifying organisms.

Methanococcoides burtonii is a methylotrophic methanogenic archaeon first isolated from Ace Lake, Antarctica. Its type strain is DSM 6242.

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.

Nitrososphaera gargensis is a non-pathogenic, small coccus measuring 0.9 ± 0.3 μm in diameter. N. gargensis is observed in small abnormal cocci groupings and uses its archaella to move via chemotaxis. Being an Archaeon, Nitrososphaera gargensis has a cell membrane composed of crenarchaeol, its isomer, and a distinct glycerol dialkyl glycerol tetraether (GDGT), which is significant in identifying ammonia-oxidizing archaea (AOA). The organism plays a role in influencing ocean communities and food production.

Crenarchaeol is a glycerol biphytanes glycerol tetraether (GDGT) biological membrane lipid. Together with archaeol, crenarcheol comprises a major component of archaeal membranes. Archaeal membranes are distinct from those of bacteria and eukaryotes because they contain isoprenoid GDGTs instead of diacyl lipids, which are found in the other domains. It has been proposed that GDGT membrane lipids are an adaptation to the high temperatures present in the environments that are home to extremophile archaea

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Further reading