Nitrosopumilus

Nitrosopumilus
Scientific classification
Domain:
Archaea
Phylum:
Nitrososphaerota
Class:
Nitrososphaeria
Order:
Nitrosopumilales
Family:
Nitrosopumilaceae
Genus:
Nitrosopumilus

Qin et al. 2017
Type species
Nitrosopumilus maritimus
Qin et al. 2017
Species
  • N. adriaticus
  • "Ca. N. aestuariumsis"
  • "Ca. N. catalinensis"
  • "N. cobalaminigenes"
  • "N. cymbastelae"
  • "N. detritiferus"
  • "N. hexadellae"
  • "Ca. N. koreensis"
  • N. maritimus
  • "N. oxyclinae"
  • N. piranensis
  • "Ca. N. salarius"
  • "Ca. N. sediminis"
  • "N. ureiphilus"
  • N. zosterae
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 Thaumarchaeota to be isolated in pure culture. Gene sequences suggest that the Group 1a Thaumarchaeota 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. N. maritimus cells are shaped like peanuts and can be found both as individuals and in loose aggregates.[2] It lives by oxidizing ammonia to nitrite. N. maritimus is capable of oxidizing ammonia at levels as low as 10 nanomolar, near the limit to sustain its life.[3] N. maritimus lives 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.

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

N. maritimus populations 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.[8] 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 Thaumarchaeota group in the water column[9].  These archaea have also been found to change their membrane's composition in relation to temperature (by GDGT cyclization), growth,[10] metabolic status,[11] and, even if less dramatically, to pH.[12]

Cell division

Euryarchaeota, Crenarchaeota, and Thaumarchaeota are the three major Phylum of Archaea which use cell division to duplicate. Euryarchaeota and Bacteria use the FtsZ mechanism in cell division, while Crenarchaeota divide using the Cvd machinery. However, Thaumarchaeota such as N. maritimus adopts both mechanisms, FtsZ and Cdv. Nevertheless, after further researches, N. maritimus was found to use mainly Cvd proteins rather than FtsZ during cell division. In this case, Cvd is the primary system in cell division for N. maritimus.[13][14] Therefore, to replicate a genome of 1.645Mb, N. maritimus spends 15 to 18 hours.[15]

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 organic carbon.[16] 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[17]

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 Thaumarchaeota 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.[18] 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.[19] 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.[20] Two hypothesis 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:[21]

•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)[22] and National Center for Biotechnology Information (NCBI)[23] Cladogram was taken from GTDB 06-RS202 (Genome Taxonomy Database).[24][25][26]

Nitrosopumilus
 
 

N. adriaticus Bayer et al. 2019

 
 

"N. ureiphilus" Qin et al. 2017

 
 
 
 
 

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

 
 
 

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

 
 
 

"N. cobalaminigenes" Qin et al. 2017

 
 

"N. oxyclinae" Qin et al. 2017

 
 
 
 
 
 

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

 
 
 

N. maritimus Qin et al. 2017

 
 
 

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

 
 

N. piranensis Bayer et al. 2019

 
 
 
 
 
 

Ecology

Habitats

Characteristic of the Thaumarchaeota 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

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 phytoplankton's production [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]

References

  1. ↑ Walker, C. B.; de la Torre, J. R.; Klotz, M. G.; Urakawa, H.; Pinel, N.; Arp, D. J.; Brochier-Armanet, C.; Chain, P. S. G.; Chan, P. P. (2010-05-11). "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 (19): 8818–8823. Bibcode:2010PNAS..107.8818W. doi:10.1073/pnas.0913533107. ISSN 1091-6490. PMC 2889351. PMID 20421470.
  2. ↑ Ko ̈nneke; Bernhard; de la Torre; Walker; Waterbury; Stahl (2005). "Isolation of an autotrophic ammonia-oxidizing marine archaeon". Nature. 437 (7058): 543–546. Bibcode:2005Natur.437..543K. doi:10.1038/nature03911. PMID 16177789. S2CID 4340386.
  3. ↑ http://www.physorg.com/news173538255.html Planet's nitrogen cycle overturned by 'tiny ammonia eater of the seas' Hannah Hickey 2009-09-30 originally based on a Nature publication by Willm Martens-Habbena, David Stahl
  4. ↑ Kraft, Beate; Jehmlich, Nico; Larsen, Morten; Bristow, Laura A.; Könneke, Martin; Thamdrup, Bo; Canfield, Donald E. (2022-01-07). "Oxygen and nitrogen production by an ammonia-oxidizing archaeon". Science. 375 (6576): 97–100. doi:10.1126/science.abe6733. ISSN 0036-8075.
  5. ↑ Könneke, Martin; Bernhard, Anne E.; de la Torre, José R.; Walker, Christopher B.; Waterbury, John B.; Stahl, David A. (22 September 2005). "Isolation of an autotrophic ammonia-oxidizing marine archaeon". Nature. 437 (7058): 543–546. Bibcode:2005Natur.437..543K. doi:10.1038/nature03911. PMID 16177789. S2CID 4340386.
  6. ↑ Elling, Felix J.; Ko ̈nneke, Martin; Mußmann, Marc; Greve, Andreas; Hinrichs, Kai-Uwe (2015). "Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates". Geochimica et Cosmochimica Acta. 171: 238. Bibcode:2015GeCoA.171..238E. doi:10.1016/j.gca.2015.09.004.
  7. ↑ Schouten, Stefan; Hopmans, Ellen C.; Baas, Marianne; Boumann, Henry; Standfest, Sonja; Ko ̈nneke, Martin; Stahl, David A.; Sinninghe Damste, Jaap S. (2008). "Intact Membrane Lipids of "Candidatus Nitrosopumilus maritimus," a Cultivated Representative of the Cosmopolitan Mesophilic Group I Crenarchaeota". Applied and Environmental Microbiology. 74 (8): 2433–2440. Bibcode:2008ApEnM..74.2433S. doi:10.1128/AEM.01709-07. PMC 2293165. PMID 18296531. S2CID 25945482.
  8. ↑ Elling, Felix J.; Ko ̈nneke, Martin; Mußmann, Marc; Greve, Andreas; Hinrichs, Kai-Uwe (2015). "Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates". Geochimica et Cosmochimica Acta. 171: 238. Bibcode:2015GeCoA.171..238E. doi:10.1016/j.gca.2015.09.004.
  9. ↑ Elling, Felix J.; Ko ̈nneke, Martin; Mußmann, Marc; Greve, Andreas; Hinrichs, Kai-Uwe (2015). "Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates". Geochimica et Cosmochimica Acta. 171: 238. Bibcode:2015GeCoA.171..238E. doi:10.1016/j.gca.2015.09.004.
  10. ↑ Elling; Ko ̈nneke; Lipp; Becker; Gagen; Hinrichs (2014). "Effects of growth phase on the membrane lipid composition of the thaumarchaeon Nitrosopumilus maritimus and their implications for archaeal lipid distributions in the marine environment". Geochimica et Cosmochimica Acta. 141: 579. Bibcode:2014GeCoA.141..579E. doi:10.1016/j.gca.2014.07.005.
  11. ↑ Huguet; Urakawa; Martens-Habbena; Truxal; Stahl; Ingalls (2009). "Intact Membrane Lipids of "Candidatus Nitrosopumilus maritimus," a Cultivated Representative of the Cosmopolitan Mesophilic Group I Crenarchaeota". Organic Geochemistry. 41: 930-934. doi:10.1016/j.orggeochem.2010.04.012.
  12. ↑ Elling, Felix J.; Ko ̈nneke, Martin; Mußmann, Marc; Greve, Andreas; Hinrichs, Kai-Uwe (2015). "Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates". Geochimica et Cosmochimica Acta. 171: 238. Bibcode:2015GeCoA.171..238E. doi:10.1016/j.gca.2015.09.004.
  13. ↑ Ng, Kian-Hong, Vinayaka Srinivas, Ramanujam Srinivasan, and Mohan Balasubramanian. ‘The Nitrosopumilus Maritimus CdvB, but Not FtsZ, Assembles into Polymers’. Archaea 2013 (2013): 1–10. https://doi.org/10.1155/2013/104147.
  14. ↑ Mosier, Annika C., Eric E. Allen, Maria Kim, Steven Ferriera, and Christopher A. Francis. ‘Genome Sequence of “ Candidatus Nitrosopumilus Salaria” BD31, an Ammonia-Oxidizing Archaeon from the San Francisco Bay Estuary’. Journal of Bacteriology 194, no. 8 (15 April 2012): 2121–22. https://doi.org/10.1128/JB.00013-12.
  15. ↑ Pelve, Erik A., Ann-Christin Lindås, Willm Martens-Habbena, José R. de la Torre, David A. Stahl, and Rolf Bernander. ‘Cdv-Based Cell Division and Cell Cycle Organization in the Thaumarchaeon Nitrosopumilus Maritimus: Cdv-Based Cell Division in N. Maritimus’. Molecular Microbiology 82, no. 3 (November 2011): 555–66. https://doi.org/10.1111/j.1365-2958.2011.07834.x.
  16. ↑ Berg, Ivan A., Daniel Kockelkorn, Wolfgang Buckel, and Georg Fuchs. ‘A 3-Hydroxypropionate/4-Hydroxybutyrate Autotrophic Carbon Dioxide Assimilation Pathway in Archaea’. Science 318, no. 5857 (14 December 2007): 1782–86. https://doi.org/10.1126/science.1149976.
  17. ↑ 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 107, no. 19 (11 May 2010): 8818–23.
  18. ↑ The ISME Journal (2019) 13:2295–2305 https://doi.org/10.1038/s41396-019-0434-8
  19. ↑ Madigan, Michael T., 1949- Brock biology of microorganisms / Michael T. Madigan. . . [et al.]. — Fourteenth edition. pages cm Includes index. ISBN 978-0-321-89739-8 1. Microbiology. I. Title. QR41.2.B77 2015 579–dc23
  20. ↑ Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea Neeraja Vajralaa,1, Willm Martens-Habbenab,1, Luis A. Sayavedra-Sotoa , Andrew Schauerc , Peter J. Bottomleyd , David A. Stahlb , and Daniel J. Arpa,2 Departments of a Botany and Plant Pathology and d Microbiology, Oregon State University, Corvallis, OR 97331; and Departments of b Civil and Environmental Engineering and c Earth and Space Science, University of Washington, Seattle, WA 98195 Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved December 7, 2012 (received for review August 17, 2012)
  21. ↑ Current Opinion in Chemical Biology 2019, 49:9–15 This review comes from a themed issue on Bioinorganic chemistry Edited by Kyle M Lancaster For a complete overview see the Issue and the Editorial Available online 17th September 2018 https://doi.org/10.1016/j.cbpa.2018.09.003 1367-5931/ã 2018 Elsevier Ltd. All rights reserved.
  22. ↑ J.P. Euzéby; et al. (1997). "Nitrosopumilus". List of Prokaryotic names with Standing in Nomenclature (LPSN). Retrieved 2021-03-20.
  23. ↑ Sayers; et al. "Nitrosopumilus". National Center for Biotechnology Information (NCBI) taxonomy database. Retrieved 2021-03-20.
  24. ↑ "GTDB release 06-RS202". Genome Taxonomy Database. Retrieved 6 December 2021.
  25. ↑ "ar122_r202.sp_label". Genome Taxonomy Database. Retrieved 6 December 2021.
  26. ↑ "Taxon History". Genome Taxonomy Database. Retrieved 6 December 2021.
  27. ↑ Brochier-Armanet, Céline, Bastien Boussau, Simonetta Gribaldo, and Patrick Forterre. “Mesophilic Crenarchaeota: Proposal for a Third Archaeal Phylum, the Thaumarchaeota.” Nature Reviews Microbiology 6, no. 3 (March 2008): 245–52. https://doi.org/10.1038/nrmicro1852.
  28. 1 2 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.
  29. 1 2 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.
  30. ↑ Karner, Markus B., Edward F. DeLong, and David M. Karl. “Archaeal Dominance in the Mesopelagic Zone of the Pacific Ocean.” Nature 409, no. 6819 (January 2001): 507–10. https://doi.org/10.1038/35054051.
  31. 1 2 3 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.
  32. 1 2 3 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.
  33. ↑ Yool, Andrew, Adrian P. Martin, Camila Fernández, and Darren R. Clark. “The Significance of Nitrification for Oceanic New Production.” Nature 447, no. 7147 (June 2007): 999–1002. https://doi.org/10.1038/nature05885.
  34. ↑ 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.

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