Nitrosopumilus Explained

Nitrosopumilus is a genus of archaea. The type species, 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.

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

All known Archaea 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 -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 oxidation

The isolation and the sequencing of N. maritimuss 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. 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 . Instead, the genome lacks the gene encoding for Hydroxylamine Oxidoreductase (HAO) responsible for oxidizing the intermediate 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, 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]

The S-layer of N. maritimus is found to form into multiple layers of channels that allow ammonium cations to flow through.[19]

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)[20] and National Center for Biotechnology Information (NCBI)[21]

Ecology

Habitats

Characteristic of the Nitrososphaerota phylum, N. maritimus[28] is mainly found in oligotrophic (poor environment in nutrients) open ocean, within the Pelagic zone.[29] Initially discovered in Seattle, in an aquarium,[30] 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.[31] N. maritimus is an aerobic archeon able to grow even with an extremely low concentration of nutrients,[32] like in dark-deep open ocean, in which N. maritimus as an important impact.[33]

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 . In fact, nitrate fuels half of the primary production of phytoplankton [34] 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.[35]

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.

See also

Further reading

Notes and 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. 10.1073/pnas.0913533107. 1091-6490. 2889351. 20421470. 2010PNAS..107.8818W. free.
  2. Ko ̈nneke . Bernhard . de la Torre . Walker . Waterbury . Stahl . Isolation of an autotrophic ammonia-oxidizing marine archaeon . Nature . 2005 . 437. 7058 . 543–546 . 10.1038/nature03911 . 16177789 . 2005Natur.437..543K . 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. en. 375. 6576. 97–100. 10.1126/science.abe6733. 0036-8075.
  5. Könneke. Martin. Bernhard. Anne E.. de la Torre. José R.. Walker. Christopher B.. Waterbury. John B.. Stahl. David A.. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 22 September 2005. 437. 7058. 543–546. 10.1038/nature03911. 16177789. 2005Natur.437..543K. 4340386.
  6. Elling . Felix J. . Ko ̈nneke . Martin . Mußmann . Marc . Greve . Andreas . Hinrichs . Kai-Uwe . Influence of temperature, pH, and salinity on membrane lipid composition and TEX86 of marine planktonic thaumarchaeal isolates . Geochimica et Cosmochimica Acta . 2015 . 171. 238 . 10.1016/j.gca.2015.09.004 . 2015GeCoA.171..238E .
  7. Schouten . Stefan . Hopmans . Ellen C. . Baas . Marianne . Boumann . Henry . Standfest . Sonja . Ko ̈nneke . Martin . Stahl . David A. . Sinninghe Damste . Jaap S. . Intact Membrane Lipids of "Candidatus Nitrosopumilus maritimus," a Cultivated Representative of the Cosmopolitan Mesophilic Group I Crenarchaeota . Applied and Environmental Microbiology . 2008 . 74 . 8. 2433–2440 . 10.1128/AEM.01709-07 . 18296531 . 2293165 . 2008ApEnM..74.2433S . 25945482 .
  8. Elling . Ko ̈nneke . Lipp . Becker . Gagen . Hinrichs . 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 . 2014 . 141. 579 . 10.1016/j.gca.2014.07.005 . 2014GeCoA.141..579E .
  9. Huguet . Urakawa . Martens-Habbena . Truxal . Stahl . Ingalls . Intact Membrane Lipids of "Candidatus Nitrosopumilus maritimus," a Cultivated Representative of the Cosmopolitan Mesophilic Group I Crenarchaeota . Organic Geochemistry . 2009 . 41 . 930–934. 10.1016/j.orggeochem.2010.04.012 .
  10. 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.
  11. 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.
  12. 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.
  13. 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.
  14. 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.
  15. The ISME Journal (2019) 13:2295–2305https://doi.org/10.1038/s41396-019-0434-8
  16. Madigan, Michael T., 1949-Brock biology of microorganisms / Michael T. Madigan. . . [et al.]. — Fourteenth edition. pages cmIncludes index.ISBN 978-0-321-89739-81. Microbiology. I. Title.QR41.2.B77 2015579–dc23
  17. Hydroxylamine as an intermediate in ammoniaoxidation by globally abundant marine archaeaNeeraja Vajralaa,1, Willm Martens-Habbenab,1, Luis A. Sayavedra-Sotoa, Andrew Schauerc, Peter J. Bottomleyd,David A. Stahlb, and Daniel J. Arpa,2Departments of aBotany and Plant Pathology and dMicrobiology, Oregon State University, Corvallis, OR 97331; and Departments of bCivil and EnvironmentalEngineering and cEarth and Space Science, University of Washington, Seattle, WA 98195Edited by Edward F. DeLong, Massachusetts Institute of Technology, Cambridge, MA, and approved December 7, 2012 (received for review August 17, 2012)
  18. Current Opinion in Chemical Biology 2019, 49:9–15This review comes from a themed issue on Bioinorganic chemistryEdited by Kyle M LancasterFor a complete overview see the Issue and the EditorialAvailable online 17 September 2018https://doi.org/10.1016/j.cbpa.2018.09.0031367-5931/ã 2018 Elsevier Ltd. All rights reserved.
  19. von Kügelgen . Andriko . Cassidy . C. Keith . van Dorst . Sofie . Pagani . Lennart L. . Batters . Christopher . Ford . Zephyr . Löwe . Jan . Alva . Vikram . Stansfeld . Phillip J. . Bharat . Tanmay A. M. . Membraneless channels sieve cations in ammonia-oxidizing marine archaea . Nature . 6 June 2024 . 630 . 8015 . 230–236 . 10.1038/s41586-024-07462-5 . free. 11153153 .
  20. Web site: J.P. Euzéby . et al. . 1997 . Nitrosopumilus . 2021-03-20 . List of Prokaryotic names with Standing in Nomenclature (LPSN).
  21. Web site: Sayers. et al.. Nitrosopumilus . 2021-03-20 . National Center for Biotechnology Information (NCBI) taxonomy database.
  22. Web site: The LTP . 10 May 2023.
  23. Web site: LTP_all tree in newick format. 10 May 2023.
  24. Web site: LTP_06_2022 Release Notes. 10 May 2023.
  25. Web site: GTDB release 08-RS214 . Genome Taxonomy Database. 10 May 2023.
  26. Web site: ar53_r214.sp_label . Genome Taxonomy Database. 10 May 2023.
  27. Web site: Taxon History . Genome Taxonomy Database. 10 May 2023.
  28. 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.
  29. 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.
  30. 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.
  31. 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.
  32. 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.
  33. 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.
  34. 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.
  35. 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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