Halobacterium salinarum

Last updated

Halobacterium salinarum
Halobacterium salinarum NRC-1.png
Halobacterium salinarum NRC-1
Size bar = 270 nm
Scientific classification
Domain:
Archaea
Phylum:
Euryarchaeota
Class:
Halobacteria
Order:
Halobacteriales
Family:
Halobacteriaceae
Genus:
Halobacterium
Species:
H. salinarum
Binomial name
Halobacterium salinarum
corrig. (Harrison and Kennedy 1922)
Elazari-Volcani 1957
Synonyms

Pseudomonas salinariaHarrison and Kennedy 1922
Serratia salinaria(Harrison and Kennedy 1922) Bergey et al. 1923
Flavobacterium (subgen. Halobacterium) salinarium(Harrison and Kennedy 1922) Elazari-volcani 1940
Halobacter salinaria(Harrison and Kennedy 1922) Anderson 1954
Halobacterium salinarium(Harrison and Kennedy 1922) Elazari-Volcani 1957
Halobacterium halobium(Petter 1931) Elazari-Volcani 1957
Halobacterium cutirubrum(Lochhead 1934) Elazari-Volcani 1957Halobacterium piscialsi(Yachai et al. 2008) [1]

Contents

Halobacterium salinarum, formerly known as Halobacterium cutirubrum or Halobacterium halobium, is an extremely halophilic marine obligate aerobic archaeon. Despite its name, this is not a bacterium, but a member of the domain Archaea. [2] It is found in salted fish, hides, hypersaline lakes, and salterns. As these salterns reach the minimum salinity limits for extreme halophiles, their waters become purple or reddish color due to the high densities of halophilic Archaea. [2] H. salinarum has also been found in high-salt food such as salt pork, marine fish, and sausages. The ability of H. salinarum to survive at such high salt concentrations has led to its classification as an extremophile.

Cell morphology and metabolism

Halobacteria are single-celled, rod-shaped microorganisms that are among the most ancient forms of life and appeared on Earth billions of years ago. The membrane consists of a single lipid bilayer surrounded by an S-layer. [3] The S-layer is made of a cell-surface glycoprotein that accounts for approximately 50% of the cell surface proteins. [4] These proteins form a lattice in the membrane. Sulfate residues are abundant on the glycan chains of the glycoprotein, giving it a negative charge. The negative charge is believed to stabilize the lattice in high-salt conditions. [5]

Amino acids are the main source of chemical energy for H. salinarum, particularly arginine and aspartate, though they are able to metabolize other amino acids, as well. [3] H. salinarum have been reported to be unable to grow on sugars, and therefore need to encode enzymes capable of performing gluconeogenesis to create sugars. Although H. salinarum is unable to catabolize glucose, the transcription factor TrmB has been proven to regulate the gluconeogenic production of sugars found on the S-layer glycoprotein.

Adaptation to extreme conditions

High salt

To survive in extremely salty environments, this archaeon—as with other halophilic Archaeal species—utilizes compatible solutes (in particular, potassium chloride) to reduce osmotic stress. [6] Potassium levels are not at equilibrium with the environment, so H. salinarum express multiple active transporters that pump potassium into the cell. [3] At extremely high salt concentrations, protein precipitation will occur. To prevent the salting out of proteins, H. salinarum encodes mainly acidic proteins. The average isoelectric point of H. salinarum proteins is 5.03. [7] These highly acidic proteins are overwhelmingly negative in charge and are able to remain in solution even at high salt concentrations. [2]

Low oxygen and phototrophy

Chemiosmotic coupling between the sun energy, bacteriorhodopsin and phosphorylation by ATP synthase (chemical energy) during photosynthesis in Halobacterium salinarum (syn. H. halobium). The archaeal cell wall is omitted. Bacteriorhodopsin chemiosmosis.gif
Chemiosmotic coupling between the sun energy, bacteriorhodopsin and phosphorylation by ATP synthase (chemical energy) during photosynthesis in Halobacterium salinarum (syn. H. halobium). The archaeal cell wall is omitted.

H. salinarum can grow to such densities in salt ponds that oxygen is quickly depleted. Though it is an obligate aerobe, it is able to survive in low-oxygen conditions by utilizing light energy. H. salinarum expresses the membrane protein bacteriorhodopsin, [10] which acts as a light-driven proton pump. It consists of two parts: the 7-transmembrane protein, bacterioopsin, and the light-sensitive cofactor, retinal. Upon absorption of a photon, retinal changes its conformation, causing a conformational change in the bacterioopsin protein, as well, which drives proton transport. [11] The proton gradient formed thereby can then be used to generate chemical energy via ATP synthase.

To obtain more oxygen, H. salinarum produce gas vesicles, which allow them to float to the surface where oxygen levels are higher and more light is available. [12] These vesicles are complex structures made of proteins encoded by at least 14 genes. [13] Gas vesicles were first discovered in H. salinarum in 1967. [14]

UV protection and color

Bacterioruberin Bacterioruberin.svg
Bacterioruberin

There is little protection from the Sun in salt ponds, so H. salinarum are often exposed to high amounts of UV radiation. To compensate, they have evolved a sophisticated DNA repair mechanism. The genome encodes DNA repair enzymes homologous to those in both bacteria and eukaryotes. [2] This allows H. salinarum to repair damage to DNA faster and more efficiently than other organisms and allows them to be much more UV-tolerant.

Its red color is due primarily to the presence of bacterioruberin, a 50 carbon carotenoid Alcohol (polyol) pigment present within the membrane of H. salinarum. The primary role of bacterioruberin in the cell is to protect against DNA damage incurred by UV light. [15] This protection is not, however, due to the ability of bacterioruberin to absorb UV light. Bacterioruberin protects the DNA by acting as an antioxidant, rather than directly blocking UV light. [16] It is able to protect the cell from reactive oxygen species produced from exposure to UV by acting as a target. The bacterioruberin radical produced is less reactive than the initial radical, and will likely react with another radical, resulting in termination of the radical chain reaction. [17]

H. salinarum has been found to be responsible for the bright pink or red appearance of some bodies of hypersaline lakes, including pink lakes, such as the lake in Melbourne's Westgate Park; with the exact colour of the lake depending on the balance between the alga Dunaliella salina and H. salinarium, with salt concentration having a direct impact. [18] [19] However, recent studies at Lake Hillier in Western Australia have shown that other bacteria, notably Salinibacter ruber , along with algal and other factors, cause the pink color of these lakes. [20] [21] [22] [23] The researchers found 10 species of halophilic bacteria and archaea as well as several species of Dunaliella algae, nearly all of which contain some pink, red or salmon-coloured pigment. [22] [21]

Protection against ionizing radiation and desiccation

H. salinarum is polyploid [24] and highly resistant to ionizing radiation and desiccation, conditions that induce DNA double-strand breaks. [25] Although chromosomes are initially shattered into many fragments, complete chromosomes are regenerated by making use of over-lapping fragments. Regeneration occurs by a process involving DNA single-stranded binding protein and is likely a form of homologous recombinational repair. [26]

Genome

Whole genome sequences are available for two strains of H. salinarum, NRC-1 [3] and R1. [27] The Halobacterium sp. NRC-1 genome consists of 2,571,010 base pairs on one large chromosome and two mini-chromosomes. The genome encodes 2,360 predicted proteins. [3] The large chromosome is very G-C rich (68%). [28] High GC-content of the genome increases stability in extreme environments. Whole proteome comparisons show the definite archaeal nature of this halophile with additional similarities to the Gram-positive Bacillus subtilis and other bacteria.

As a model organism

H. salinarum is as easy to culture as E. coli and serves as an excellent model system. Methods for gene replacement and systematic knockout have been developed, [29] so H. salinarum is an ideal candidate for the study of archaeal genetics and functional genomics.

For hydrogen production

Hydrogen production using H. salinarum coupled to a hydrogenase donor like E. coli are reported in literature. [30]

Oldest DNA ever recovered

A sample of encapsulated inments from a close genetic relative of H. salinarum is estimated to be 121 million years old[ citation needed ]. Oddly, the material had also been recovered previously, but it was so similar to that of the modern descendants that the scientists who examined those earlier samples had mistakenly identified them as such, albeit contaminated.[ citation needed ]

Scientists have previously recovered similar genetic material from the Michigan Basin,[ clarification needed ] the same region where the latest discovery was made. But that DNA, discovered in a salt-cured buffalo hide in the 1930s, was so similar to that of modern microbes that many scientists believed the samples had been contaminated. [31] The curing salt had been derived from a mine in Saskatchewan, the site of the most recent sample described by Jong Soo Park of Dalhousie University in Halifax, Nova Scotia, Canada. [32]

Russell Vreeland of Ancient Biomaterials Institute of West Chester University in Pennsylvania, USA, performed an analysis of all known types of halophilic bacteria, which yielded the finding that Park's bacteria contained six segments of DNA never seen before in halophiles. Vreeland also tracked down the buffalo skin and determined that the salt came from the same mine as Park's sample. He has also discovered an even older halophile estimated at 250 million years old in New Mexico. [33] However, his findings date the crystal surrounding the bacteria, and DNA analysis suggests the bacteria themselves are likely to be less ancient. [34]

Related Research Articles

A halophile is an extremophile that thrives in high salt concentrations. In chemical terms, halophile refers to a Lewis acidic species that has some ability to extract halides from other chemical species.

<i>Halobacterium</i> Genus of archaea

Halobacterium is a genus in the family Halobacteriaceae.

Halobacteriaceae is a family in the order Halobacteriales and the domain Archaea. Halobacteriaceae represent a large part of halophilic Archaea, along with members in two other methanogenic families, Methanosarcinaceae and Methanocalculaceae. The family consists of many diverse genera that can survive extreme environmental niches. Most commonly, Halobacteriaceae are found in hypersaline lakes and can even tolerate sites polluted by heavy metals. They include neutrophiles, acidophiles, alkaliphiles, and there have even been psychrotolerant species discovered. Some members have been known to live aerobically, as well as anaerobically, and they come in many different morphologies. These diverse morphologies include rods in genus Halobacterium, cocci in Halococcus, flattened discs or cups in Haloferax, and other shapes ranging from flattened triangles in Haloarcula to squares in Haloquadratum, and Natronorubrum. Most species of Halobacteriaceae are best known for their high salt tolerance and red-pink pigmented members, but there are also non-pigmented species and those that require moderate salt conditions. Some species of Halobacteriaceae have been shown to exhibit phosphorus solubilizing activities that contribute to phosphorus cycling in hypersaline environments. Techniques such as 16S rRNA analysis and DNA-DNA hybridization have been major contributors to taxonomic classification in Halobacteriaceae, partly due to the difficulty in culturing halophilic Archaea.

<span class="mw-page-title-main">Halobacteriales</span> Order of archaea

Halobacteriales are an order of the Halobacteria, found in water saturated or nearly saturated with salt. They are also called halophiles, though this name is also used for other organisms which live in somewhat less concentrated salt water. They are common in most environments where large amounts of salt, moisture, and organic material are available. Large blooms appear reddish, from the pigment bacteriorhodopsin. This pigment is used to absorb light, which provides energy to create ATP. Halobacteria also possess a second pigment, halorhodopsin, which pumps in chloride ions in response to photons, creating a voltage gradient and assisting in the production of energy from light. The process is unrelated to other forms of photosynthesis involving electron transport; however, and halobacteria are incapable of fixing carbon from carbon dioxide.

<span class="mw-page-title-main">Haloarchaea</span> Class of salt-tolerant archaea

Haloarchaea are a class of the Euryarchaeota, found in water saturated or nearly saturated with salt. Halobacteria are now recognized as archaea rather than bacteria and are one of the largest groups. The name 'halobacteria' was assigned to this group of organisms before the existence of the domain Archaea was realized, and while valid according to taxonomic rules, should be updated. Halophilic archaea are generally referred to as haloarchaea to distinguish them from halophilic bacteria.

<span class="mw-page-title-main">Sulfolobales</span> Order of archaea

Sulfolobales is an order of archaeans in the class Thermoprotei.

<i>Haloarcula</i> Genus of archaea

Haloarcula is a genus of extreme halophilic Archaea in the class of Halobactaria.

Halocins are bacteriocins produced by halophilic Archaea and a type of archaeocin.

<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">Pink lake</span> Pink lake phenomenon and examples

A pink lake is a lake that has a red or pink colour. This is often caused by the presence of salt-tolerant algae that produces carotenoids, such as Dunaliella salina, usually in conjunction with specific bacteria and archaea, which may vary from lake to lake. The most common archaeon is Halobacterium salinarum.

The archaellum is a unique structure on the cell surface of many archaea that allows for swimming motility. The archaellum consists of a rigid helical filament that is attached to the cell membrane by a molecular motor. This molecular motor – composed of cytosolic, membrane, and pseudo-periplasmic proteins – is responsible for the assembly of the filament and, once assembled, for its rotation. The rotation of the filament propels archaeal cells in liquid medium, in a manner similar to the propeller of a boat. The bacterial analog of the archaellum is the flagellum, which is also responsible for their swimming motility and can also be compared to a rotating corkscrew. Although the movement of archaella and flagella is sometimes described as "whip-like", this is incorrect, as only cilia from Eukaryotes move in this manner. Indeed, even "flagellum" is a misnomer, as bacterial flagella also work as propeller-like structures.

<i>Haloferax volcanii</i> Species of Halobacteria

Haloferax volcanii is a species of organism in the genus Haloferax in the Archaea.

<i>Methanohalophilus mahii</i> Species of archaeon

Methanohalophilus mahii is an obligately anaerobic, methylotrophic, methanogenic cocci-shaped archaeon of the genus Methanohalophilus that can be found in high salinity aquatic environments. The name Methanohalophilus is said to be derived from methanum meaning "methane" in Latin; halo meaning "salt" in Greek; and mahii meaning "of Mah" in Latin, after R.A. Mah, who did substantial amounts of research on aerobic and methanogenic microbes. The proper word in ancient Greek for "salt" is however hals (ἅλς). The specific strain type was designated SLP and is currently the only identified strain of this species.

Halobacterium noricense is a halophilic, rod-shaped microorganism that thrives in environments with salt levels near saturation. Despite the implication of the name, Halobacterium is actually a genus of archaea, not bacteria. H. noricense can be isolated from environments with high salinity such as the Dead Sea and the Great Salt Lake in Utah. Members of the Halobacterium genus are excellent model organisms for DNA replication and transcription due to the stability of their proteins and polymerases when exposed to high temperatures. To be classified in the genus Halobacterium, a microorganism must exhibit a membrane composition consisting of ether-linked phosphoglycerides and glycolipids.

Salinibacter ruber is an extremely halophilic red bacterium, first found in Spain in 2002.

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

Shiladitya DasSarma is a molecular biologist well-known for contributions to the biology of halophilic and extremophilic microorganisms. He is a Professor in the University of Maryland Baltimore. He earned a PhD degree in biochemistry from the Massachusetts Institute of Technology and a BS degree in chemistry from Indiana University Bloomington. Prior to taking a faculty position, he conducted research at the Massachusetts General Hospital, Harvard Medical School, and Pasteur Institute, Paris.

Haloarcula marismortui is a halophilic archaeon isolated from the Dead Sea

<i>Haloferax mediterranei</i> Species of bacterium

Haloferax mediterranei is a species of archaea in the family Haloferacaceae.

<span class="mw-page-title-main">Archaerhodopsin</span> Family of archaea

Archaerhodopsin proteins are a family of retinal-containing photoreceptors found in the archaea genera Halobacterium and Halorubrum. Like the homologous bacteriorhodopsin (bR) protein, archaerhodopsins harvest energy from sunlight to pump H+ ions out of the cell, establishing a proton motive force that is used for ATP synthesis. They have some structural similarities to the mammalian GPCR protein rhodopsin, but are not true homologs.

Natrialbales is an order of halophilic, chemoorganotrophic archaea within the class Haloarchaea. The type genus of this order is Natrialba.

References

  1. ↑ Minegishi H, Echigo A, Shimane Y, Kamekura M, Tanasupawat S, Visessanguan W, Usami R (September 2012). "Halobacterium piscisalsi Yachai et al. 2008 is a later heterotypic synonym of Halobacterium salinarum Elazari-Volcani 1957". International Journal of Systematic and Evolutionary Microbiology. 62 (Pt 9): 2160–2162. doi:10.1099/ijs.0.036905-0. PMID   22058320.
  2. 1 2 3 4 Dassarma, Shiladitya (2007). "Extreme Microbes". American Scientist. 95 (3): 224. doi:10.1511/2007.65.224.
  3. 1 2 3 4 5 Ng, W. V.; Kennedy, S. P.; et al. (2000). "Genome sequence of Halobacterium species NRC-1". Proceedings of the National Academy of Sciences. 97 (22): 12176–81. Bibcode:2000PNAS...9712176N. doi: 10.1073/pnas.190337797 . PMC   17314 . PMID   11016950.
  4. ↑ Mescher, M. F.; Strominger, J. L. (1976). "Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium". The Journal of Biological Chemistry. 251 (7): 2005–14. doi: 10.1016/S0021-9258(17)33647-5 . PMID   1270419.
  5. ↑ Sára, M; Sleytr, U. B. (2000). "S-Layer proteins". Journal of Bacteriology. 182 (4): 859–68. doi:10.1128/jb.182.4.859-868.2000. PMC   94357 . PMID   10648507.
  6. ↑ Pérez-Fillol, M; Rodríguez-Valera, F (1986). "Potassium ion accumulation in cells of different halobacteria". Microbiología. 2 (2): 73–80. PMID   3271061.
  7. ↑ Kozlowski, LP (26 October 2016). "Proteome-pI: proteome isoelectric point database". Nucleic Acids Research. 45 (D1): D1112–D1116. doi:10.1093/nar/gkw978. PMC   5210655 . PMID   27789699.
  8. ↑ Nicholls D. G.; Ferguson S. J. (1992). Bioenergetics 2 (2nd ed.). San Diego: Academic Press. ISBN   9780125181242.
  9. ↑ Stryer, Lubert (1995). Biochemistry (fourth ed.). New York – Basingstoke: W. H. Freeman and Company. ISBN   978-0716720096.
  10. ↑ Oesterhelt, D; Stoeckenius, W (1973). "Functions of a new photoreceptor membrane". Proceedings of the National Academy of Sciences of the United States of America. 70 (10): 2853–7. Bibcode:1973PNAS...70.2853O. doi: 10.1073/pnas.70.10.2853 . PMC   427124 . PMID   4517939.
  11. ↑ Andersson, M; Malmerberg, E; Westenhoff, S; Katona, G; Cammarata, M; Wöhri, A. B.; Johansson, L. C.; Ewald, F; Eklund, M; Wulff, M; Davidsson, J; Neutze, R (2009). "Structural dynamics of light-driven proton pumps". Structure. 17 (9): 1265–75. doi: 10.1016/j.str.2009.07.007 . PMID   19748347.
  12. ↑ Oren, A., Ecology of extremely halophilic microorganisms, Vreeland, R.H., Hochstein, L.I., editors, The Biology of Halophilic Bacteria, CRC Press, Inc., Boca Raton, Florida, 1993, p. 25–54.
  13. ↑ Walsby, A. E. (1994). "Gas vesicles". Microbiological Reviews. 58 (1): 94–144. doi:10.1128/mmbr.58.1.94-144.1994. PMC   372955 . PMID   8177173.
  14. ↑ Larsen, H; Omang, S; Steensland, H (1967). "On the gas vacuoles of the halobacteria". Archiv für Mikrobiologie. 59 (1): 197–203. doi:10.1007/bf00406332. PMID   5602456. S2CID   20107779.
  15. ↑ Shahmohammadi, H. R.; Asgarani, E; et al. (1998). "Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents". Journal of Radiation Research. 39 (4): 251–62. Bibcode:1998JRadR..39..251S. doi: 10.1269/jrr.39.251 . PMID   10196780.
  16. ↑ Ide, H., Takeshi, S., Hiroaki, T., Studies on the antioxidation activity of bacterioruberin, Urakami Found Mem, 1998, 6:127–33.
  17. ↑ Saito, T., Miyabe, Y., Ide, H., Yamamoto, O., Hydroxyl radical scavenging ability of bacterioruberin, Radiat Phys Chem, 1997, 50(3):267–9.
  18. ↑ "Westgate Park's Pink Lake". ToMelbourne.com.au. 8 July 2018. Retrieved 23 January 2022.
  19. ↑ "Pink Lake In The Fringe of CBD". Pink Lake In The Fringe of CBD (in Afrikaans). Retrieved 23 January 2022.
  20. ↑ Salleh, Anna (4 January 2022). "Why Australia has so many pink lakes and why some of them are losing their colour". ABC News. ABC Science. Australian Broadcasting Corporation . Retrieved 21 January 2022.
  21. 1 2 "Here's the Real Reason Why Australia Has Bubblegum Pink Lakes". Discovery. 24 December 2019. Retrieved 22 January 2022.
  22. 1 2 "Why is Pink Lake on Middle Island, off the coast of Esperance, pink?". Australia's Golden Outback. Includes extract from Australian Geographic article. 18 January 2021. Retrieved 22 January 2022.{{cite web}}: CS1 maint: others (link)
  23. ↑ Cassella, Carly (13 December 2016). "How an Australian lake turned bubble-gum pink". Australian Geographic. Retrieved 22 January 2022.
  24. ↑ Soppa J (2011). "Ploidy and gene conversion in Archaea". Biochem. Soc. Trans. 39 (1): 150–4. doi:10.1042/BST0390150. PMID   21265763.
  25. ↑ Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J (2005). "Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation" (PDF). Extremophiles. 9 (3): 219–27. doi:10.1007/s00792-005-0437-4. PMID   15844015. S2CID   8391234.
  26. ↑ DeVeaux LC, Müller JA, Smith J, Petrisko J, Wells DP, DasSarma S (2007). "Extremely radiation-resistant mutants of a halophilic archaeon with increased single-stranded DNA-binding protein (RPA) gene expression". Radiat. Res. 168 (4): 507–14. Bibcode:2007RadR..168..507D. doi: 10.1667/RR0935.1 . PMID   17903038. S2CID   22393850.
  27. ↑ Pfeiffer, F; Schuster, S. C.; Broicher, A; Falb, M; Palm, P; Rodewald, K; Ruepp, A; Soppa, J; Tittor, J; Oesterhelt, D (2008). "Evolution in the laboratory: The genome of Halobacterium salinarum strain R1 compared to that of strain NRC-1". Genomics. 91 (4): 335–46. doi: 10.1016/j.ygeno.2008.01.001 . PMID   18313895.
  28. ↑ Joshi, J. G.; Guild, W. R.; Handler, P (1963). "The presence of two species of DNA in some halobacteria". Journal of Molecular Biology. 6: 34–8. doi:10.1016/s0022-2836(63)80079-0. PMID   13964964.
  29. ↑ Peck, R. F.; Dassarma, S; Krebs, M. P. (2000). "Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker". Molecular Microbiology. 35 (3): 667–76. doi: 10.1046/j.1365-2958.2000.01739.x . PMID   10672188.
  30. ↑ Brijesh Rajanandam, K S; Siva Kiran, R R (2011). "Optimization of hydrogen production by Halobacterium salinarium coupled with E coli using milk plasma as fermentative substrate". Journal of Biochemical Technology. 3 (2): 242–244. ISSN   0974-2328.
  31. ↑ Reilly, Michael; The Discovery Channel. "World's oldest known DNA discovered" . Retrieved 3 September 2010.
  32. ↑ Park, J. S.; Vreeland, R. H.; Cho, B. C.; Lowenstein, T. K.; Timofeeff, M. N. & Rosenweig, W. D. (December 2009). "Haloarchaeal diversity in 23, 121 and 419 MYA salts". Geobiology. 7 (5): 515–23. doi:10.1111/j.1472-4669.2009.00218.x. PMID   19849725.
  33. ↑ Vreeland, H; Rosenzweig, W D; Lowenstein, T; Satterfield, C; Ventosa, A (December 2006). "Fatty acid and DNA analyses of Permian bacteria isolated from ancient salt crystals reveal differences from their modern relatives". Extremophiles. 10 (1): 71–8. doi:10.1007/s00792-005-0474-z. PMID   16133658. S2CID   25102006.
  34. ↑ Graur, Dan; Pupko, Tal (2001-02-15). "The Permian Bacterium that Isn't". Molecular Biology and Evolution. Oxford Journals. 18 (6): 1143–1146. doi: 10.1093/oxfordjournals.molbev.a003887 . PMID   11371604.

Further reading

This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.