''Nitrosopumilus maritimus'' is an extremely common

archaeon Archaea ( ; singular archaeon ) 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 (in the Archaebact ...

living in seawater. It is the first member of the Group 1a

Nitrososphaerota The Nitrososphaerota (syn. Thaumarchaeota) 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 Thermoprote ...

(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. 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. They oxidize

ammonia Ammonia is an inorganic compound of nitrogen and hydrogen with the formula . A stable binary hydride, and the simplest pnictogen hydride, ammonia is a colourless gas with a distinct pungent smell. Biologically, it is a common nitrogenous was ...

nitrite The nitrite polyatomic ion, ion has the chemical formula . Nitrite (mostly sodium nitrite) is widely used throughout chemical and pharmaceutical industries. The nitrite anion is a pervasive intermediate in the nitrogen cycle in nature. The name ...

and members of ''N. maritimus'' can oxidize ammonia at levels as low as 10 nanomolar, near the limit to sustain its life. 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. ''N. maritimus'' is thus among organisms which are able to produce oxygen in dark. This organism was isolated from sediment in a tropical tank at the

Seattle Aquarium The Seattle Aquarium is a public aquarium in Seattle, Washington, United States, located on Pier 59 on the Elliott Bay waterfront. It opened in 1977 and has been accredited by the Association of Zoos and Aquariums (AZA). History Plans for a ci ...

by a group led by David Stahl (

University of Washington The University of Washington (UW, simply Washington, or informally U-Dub) is a public research university in Seattle, Washington. Founded in 1861, Washington is one of the oldest universities on the West Coast; it was established in Seattle a ...

Biology

Lipid membranes

Populations of ''N. maritimus'' are probably the main source of

glycerol dialkyl glycerol tetraether Glycerol dialkyl glycerol tetraether lipids (GDGTs) are a class of membrane lipids synthesized by archaea and some bacteria, making them useful biomarkers for these organisms in the geological record. Their presence, structure, and relative abundan ...

s (GDGTs) in the ocean, a compound which constitutes their monolayer lipidic cell membranes as intact polar lipids (IPLs) together with crenarcheol. This membrane structure is thought to maximise

proton motive force Chemiosmosis is the movement of ions across a semipermeable membrane bound structure, down their electrochemical gradient. An important example is the formation of adenosine triphosphate (ATP) by the movement of hydrogen ions (H+) across a membra ...

. The compounds found in the membrane of these organisms, such as GDGTs, IPLs, and crenarcheol, can be useful as

biomarkers In biomedical contexts, a biomarker, or biological marker, is a measurable indicator of some biological state or condition. Biomarkers are often measured and evaluated using blood, urine, or soft tissues to examine normal biological processes, p ...

for the presence of organisms belonging to the

group in the water column. These archaea have also been found to change their membrane's composition in relation to temperature (by GDGT cyclization), growth, metabolic status, and, even if less dramatically, to pH.

Cell division

Euryarchaeota Euryarchaeota (from Ancient Greek ''εὐρύς'' eurús, "broad, wide") is a phylum of archaea. Euryarchaeota are highly diverse and include methanogens, which produce methane and are often found in intestines, halobacteria, which survive extre ...

Thermoproteota The Thermoproteota (also known as crenarchaea) are archaea that have been classified as a phylum of the Archaea domain. Initially, the Thermoproteota were thought to be sulfur-dependent extremophiles but recent studies have identified characteris ...

, and

are some of the three major phyla of Archaea which use

cell division Cell division is the process by which a parent cell (biology), cell divides into two daughter cells. Cell division usually occurs as part of a larger cell cycle in which the cell grows and replicates its chromosome(s) before dividing. In eukar ...

to duplicate.

and

Bacteria Bacteria (; singular: bacterium) are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were among ...

use the

FtsZ FtsZ is a protein encoded by the ''ftsZ'' gene that assembles into a ring at the future site of bacterial cell division (also called the Z ring). FtsZ is a prokaryotic homologue of the eukaryotic protein tubulin. The initials FtsZ mean "Filamen ...

mechanism in

, while

divide using the Cvd machinery. However,

such as ''N. maritimus'' adopts both mechanisms,

and Cdv. Nevertheless, after further researches, ''N. maritimus'' was found to use mainly Cvd proteins rather than

during

. In this case, Cvd is the primary system in

for ''N. maritimus''. Therefore, to replicate a

genome In the fields of molecular biology and genetics, a genome is all the genetic information of an organism. It consists of nucleotide sequences of DNA (or RNA in RNA viruses). The nuclear genome includes protein-coding genes and non-coding ge ...

of 1.645Mb, ''N. maritimus'' spends 15 to 18 hours.

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 -fixing enzyme ribulose bisphosphate carboxylase/oxygenase (

RubisCO Ribulose-1,5-bisphosphate carboxylase-oxygenase, commonly known by the abbreviations RuBisCo, rubisco, RuBPCase, or RuBPco, is an enzyme () involved in the first major step of carbon fixation, a process by which atmospheric carbon dioxide is con ...

) 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. Using the 3-hydroxypropionate/4-hydroxybutyrate pathway method instead of the

Calvin cycle The Calvin cycle, light-independent reactions, bio synthetic phase, dark reactions, or photosynthetic carbon reduction (PCR) cycle of photosynthesis is a series of chemical reactions that convert carbon dioxide and hydrogen-carrier compounds into ...

, ''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

Ammonia Oxidizing

The isolation and the sequencing of ''N. maritimuss genome have allowed to extend the insight into the

physiology Physiology (; ) is the scientific study of functions and mechanisms in a living system. As a sub-discipline of biology, physiology focuses on how organisms, organ systems, individual organs, cells, and biomolecules carry out the chemical ...

of the organisms belonging to the

group. ''N. maritimus'' was the first

Archaeon Archaea ( ; singular archaeon ) 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 (in the Archaebact ...

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. The physiology of ''N. maritimus'' remains unclear under certain aspects. It conserves energy for its vital functions, from the

oxidation Redox (reduction–oxidation, , ) is a type of chemical reaction in which the oxidation states of substrate change. Oxidation is the loss of electrons or an increase in the oxidation state, while reduction is the gain of electrons or a d ...

of Ammonia and the reduction of Oxygen, with the formation of Nitrite. is the carbon source. It is fixed and assimilated by the microorganism through the 3-hydroxypropinate/4-hydroxybutyrate carbon cycle. ''N. maritimus'' carries out the first step of

Nitrification ''Nitrification'' is the biological oxidation of ammonia to nitrite followed by the oxidation of the nitrite to nitrate occurring through separate organisms or direct ammonia oxidation to nitrate in comammox bacteria. The transformation of amm ...

, by acting in a key role in the

Nitrogen cycle The nitrogen cycle is the biogeochemical cycle by which nitrogen is converted into multiple chemical forms as it circulates among atmospheric, terrestrial, and marine ecosystems. The conversion of nitrogen can be carried out through both biologi ...

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

(HAO) responsible for oxidizing the intermediate (NH2OH) to nitrite. The hydroxylamine is produced as a

metabolite In biochemistry, a metabolite is an intermediate or end product of metabolism. The term is usually used for small molecules. Metabolites have various functions, including fuel, structure, signaling, stimulatory and inhibitory effects on enzymes, c ...

, 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. Two hypothesis are suggested for the metabolic pathway of ''N. maritimus'' that involve two types of

enzymes Enzymes () are proteins that act as biological catalysts by accelerating chemical reactions. The molecules upon which enzymes may act are called substrate (chemistry), substrates, and the enzyme converts the substrates into different molecule ...

: the copper-based enzyme (Cu-ME) and the nitrite reductase enzyme (nirK) and its reverse: •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 ATP synthase is a protein that catalyzes the formation of the energy storage molecule adenosine triphosphate (ATP) using adenosine diphosphate (ADP) and inorganic phosphate (Pi). It is classified under ligases as it changes ADP by the formation ...

. •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 A greenhouse gas (GHG or GhG) is a gas that Absorption (electromagnetic radiation), absorbs and Emission (electromagnetic radiation), emits radiant energy within the thermal infrared range, causing the greenhouse effect. The primary greenhouse ...

that likely is produced as result of abiotic

denitrification 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 denitr ...

of metabolites.

Taxonomy

The currently accepted taxonomy is based on the

List of Prokaryotic names with Standing in Nomenclature List of Prokaryotic names with Standing in Nomenclature (LPSN) is an online database that maintains information on the naming and taxonomy of prokaryotes, following the taxonomy requirements and rulings of the International Code of Nomenclature ...

(LPSN) and

National Center for Biotechnology Information The National Center for Biotechnology Information (NCBI) is part of the United States National Library of Medicine (NLM), a branch of the National Institutes of Health (NIH). It is approved and funded by the government of the United States. The ...

(NCBI) Cladogram was taken from GTDB release 07-RS207 (8 April 2022).

Ecology

Habitats

Characteristic of the

phylum, ''N. maritimus'' is mainly found in oligotrophic (poor environment in nutrients) open ocean, within the Pelagic zone.Walker, C. B., J. R. de la Torre, M. G. Klotz, H. Urakawa, N. Pinel, D. J. Arp, C. Brochier-Armanet, et al. “Nitrosopumilus Maritimus Genome Reveals Unique Mechanisms for Nitrification and Autotrophy in Globally Distributed Marine Crenarchaea.” Proceedings of the National Academy of Sciences of the United States of America 107, no. 19 (May 11, 2010): 8818–23. https://doi.org/10.1073/pnas.0913533107. Initially discovered in Seattle, in an aquarium,Könneke, Martin, Anne E. Bernhard, José R. de la Torre, Christopher B. Walker, John B. Waterbury, and David A. Stahl. “Isolation of an Autotrophic Ammonia-Oxidizing Marine Archaeon.” Nature 437, no. 7058 (September 2005): 543–46. https://doi.org/10.1038/nature03911. 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. ''N. maritimus'' is an aerobic archeon able to grow even with an extremely low concentration of nutrients,Martens-Habbena, Willm, Paul M. Berube, Hidetoshi Urakawa, José R. de la Torre, and David A. Stahl. “Ammonia Oxidation Kinetics Determine Niche Separation of Nitrifying Archaea and Bacteria.” Nature 461, no. 7266 (October 2009): 976–79. like in dark-deep open ocean, in which ''N. maritimus'' as an important impact.Meador, Travis B., Niels Schoffelen, Timothy G. Ferdelman, Osmond Rebello, Alexander Khachikyan, and Martin Könneke. “Carbon Recycling Efficiency and Phosphate Turnover by Marine Nitrifying Archaea.” Science Advances 6, no. 19 (May 8, 2020): eaba1799. https://doi.org/10.1126/sciadv.aba1799.

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 The nitrogen cycle is the biogeochemical cycle by which nitrogen is converted into multiple chemical forms as it circulates among atmospheric, terrestrial, and marine ecosystems. The conversion of nitrogen can be carried out through both biologi ...

. 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 . In fact, nitrate fuels half of the primary production of phytoplankton but not only phytoplankton needs nitrate. The high ammonia's affinity allows ''N. maritimus'' to largely compete with the other marine phototrophs and chemotrophs. 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. Computing these two observations nitrification by ''N. maritimus'' plays a key role in the marine nitrogen cycle.Wuchter, Cornelia, Ben Abbas, Marco J. L. Coolen, Lydie Herfort, Judith van Bleijswijk, Peer Timmers, Marc Strous, et al. “Archaeal Nitrification in the Ocean.” Proceedings of the National Academy of Sciences of the United States of America 103, no. 33 (August 15, 2006): 12317–22. https://doi.org/10.1073/pnas.0600756103.

Carbon and phosphorus implications

Its ability to fix inorganic carbon via an alternative pathway (3-hydroxypropionate/4-hydroxybutyrate pathway) allows ''N. maritimus'' to participate efficiently in the flux of the global carbon budget. 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.

References

External links

{{Taxonbar, from=Q5361604 Archaea genera Candidatus taxa Marine microorganisms