Halobacterium salinarum

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.{{cite journal | pmid = 11016950 | pmc = 17314 | year = 2000 | last1 = Ng | first1 = W. V. | title = Genome sequence of Halobacterium species NRC-1 | journal = Proceedings of the National Academy of Sciences | volume = 97 | issue = 22 | pages = 12176–81 | last2 = Kennedy | first2 = S. P. | last3 = Mahairas | first3 = G. G. | last4 = Berquist | first4 = B | last5 = Pan | first5 = M | last6 = Shukla | first6 = H. D. | last7 = Lasky | first7 = S. R. | last8 = Baliga | first8 = N. S. | last9 = Thorsson | first9 = V | last10 = Sbrogna | first10 = J | last11 = Swartzell | first11 = S | last12 = Weir | first12 = D | last13 = Hall | first13 = J | last14 = Dahl | first14 = T. A. | last15 = Welti | first15 = R | last16 = Goo | first16 = Y. A. | author17 = ((Leithauser, B)) | last18 = Keller | first18 = K | last19 = Cruz | first19 = R | last20 = Danson | first20 = M. J. | last21 = Hough | first21 = D. W. | last22 = Maddocks | first22 = D. G. | last23 = Jablonski | first23 = P. E. | last24 = Krebs | first24 = M. P. | last25 = Angevine | first25 = C. M. | last26 = Dale | first26 = H | last27 = Isenbarger | first27 = T. A. | last28 = Peck | first28 = R. F. | last29 = Pohlschroder | first29 = M | last30 = Spudich | first30 = J. L. | display-authors = 2 | doi = 10.1073/pnas.190337797 | bibcode = 2000PNAS...9712176N | doi-access = free }} The S-layer is made of a cell-surface glycoprotein that accounts for approximately 50% of the cell surface proteins.{{cite journal | pmid = 1270419 | year = 1976 | last1 = Mescher | first1 = M. F. | title = Purification and characterization of a prokaryotic glucoprotein from the cell envelope of Halobacterium salinarium | journal = The Journal of Biological Chemistry | volume = 251 | issue = 7 | pages = 2005–14 | last2 = Strominger | first2 = J. L. | doi = 10.1016/S0021-9258(17)33647-5 | doi-access = free }} 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.{{cite journal | pmid = 10648507 | pmc = 94357 | year = 2000 | last1 = Sára | first1 = M | title = S-Layer proteins | journal = Journal of Bacteriology | volume = 182 | issue = 4 | pages = 859–68 | last2 = Sleytr | first2 = U. B. | doi=10.1128/jb.182.4.859-868.2000}}

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. 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.

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.{{cite journal | pmid = 3271061 | year = 1986 | last1 = Pérez-Fillol | first1 = M | title = Potassium ion accumulation in cells of different halobacteria | journal = Microbiología | volume = 2 | issue = 2 | pages = 73–80 | last2 = Rodríguez-Valera | first2 = F }} Potassium levels are not at equilibrium with the environment, so H. salinarum express multiple active transporters that pump potassium into the cell.

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.{{cite journal|last1=Kozlowski|first1=LP|title=Proteome-pI: proteome isoelectric point database.|journal=Nucleic Acids Research|date=26 October 2016|doi=10.1093/nar/gkw978|pmid=27789699|url=http://isoelectricpointdb.org/54/UP000000554_64091_all_isoelectric_point_proteome_Halobacterium_salinarum_strain_ATCC_700922_JCM_11081_NRC_1_Halobacterium_halobium.html|volume=45|issue=D1|pmc=5210655|pages=D1112–D1116}} These highly acidic proteins are overwhelmingly negative in charge and are able to remain in solution even at high salt concentrations.

File:Bacteriorhodopsin chemiosmosis.gif 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.{{cite book |title=Bioenergetics 2 |edition=2nd |author=Nicholls D. G. |author2=Ferguson S. J. |date=1992 |publisher=Academic Press |location=San Diego |isbn=9780125181242 |url-access=registration |url=https://archive.org/details/bioenergetics200nich }}{{cite book |last=Stryer |first=Lubert |date=1995 |title=Biochemistry |publisher=W. H. Freeman and Company |location=New York – Basingstoke |edition=fourth |isbn=978-0716720096 }}]]

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,{{cite journal | pmid = 4517939 | pmc = 427124 | year = 1973 | last1 = Oesterhelt | first1 = D | title = Functions of a new photoreceptor membrane | journal = Proceedings of the National Academy of Sciences of the United States of America | volume = 70 | issue = 10 | pages = 2853–7 | last2 = Stoeckenius | first2 = W | doi=10.1073/pnas.70.10.2853| bibcode = 1973PNAS...70.2853O | doi-access = free }} 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.{{cite journal | pmid = 19748347 | year = 2009 | last1 = Andersson | first1 = M | title = Structural dynamics of light-driven proton pumps | journal = Structure | volume = 17 | issue = 9 | pages = 1265–75 | last2 = Malmerberg | first2 = E | last3 = Westenhoff | first3 = S | last4 = Katona | first4 = G | last5 = Cammarata | first5 = M | last6 = Wöhri | first6 = A. B. | last7 = Johansson | first7 = L. C. | last8 = Ewald | first8 = F | last9 = Eklund | first9 = M | last10 = Wulff | first10 = M | last11 = Davidsson | first11 = J | last12 = Neutze | first12 = R | doi = 10.1016/j.str.2009.07.007 | doi-access = free }} 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.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. These vesicles are complex structures made of proteins encoded by at least 14 genes.{{cite journal | pmid = 8177173 | pmc = 372955 | year = 1994 | last1 = Walsby | first1 = A. E. | title = Gas vesicles | journal = Microbiological Reviews | volume = 58 | issue = 1 | pages = 94–144 | doi = 10.1128/mmbr.58.1.94-144.1994 }} Gas vesicles were first discovered in H. salinarum in 1967.{{cite journal | pmid = 5602456 | year = 1967 | last1 = Larsen | first1 = H | title = On the gas vacuoles of the halobacteria | journal = Archiv für Mikrobiologie | volume = 59 | issue = 1 | pages = 197–203 | last2 = Omang | first2 = S | last3 = Steensland | first3 = H | doi=10.1007/bf00406332| s2cid = 20107779 }}

File:Bacterioruberin.svg

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. 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.{{cite journal | pmid = 10196780 | year = 1998 | last1 = Shahmohammadi | first1 = H. R. | title = Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents | journal = Journal of Radiation Research | volume = 39 | issue = 4 | pages = 251–62 | last2 = Asgarani | first2 = E | last3 = Terato | first3 = H | last4 = Saito | first4 = T | last5 = Ohyama | first5 = Y | last6 = Gekko | first6 = K | last7 = Yamamoto | first7 = O | last8 = Ide | first8 = H | doi=10.1269/jrr.39.251| bibcode = 1998JRadR..39..251S | doi-access = free|display-authors=2 }} 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.Ide, H., Takeshi, S., Hiroaki, T., Studies on the antioxidation activity of bacterioruberin, Urakami Found Mem, 1998, 6:127–33. 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.Saito, T., Miyabe, Y., Ide, H., Yamamoto, O., Hydroxyl radical scavenging ability of bacterioruberin, Radiat Phys Chem, 1997, 50(3):267–9.

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.{{cite web | title=Westgate Park’s Pink Lake | website=ToMelbourne.com.au | date=8 July 2018 | url=https://tomelbourne.com.au/westgate-parks-pink-lake/ | access-date=23 January 2022}}{{cite web | title=Pink Lake In The Fringe of CBD | website=Pink Lake In The Fringe of CBD | url=https://www.weekendnotes.com/pink-lake-westgate-park/ | language=af | access-date=23 January 2022}} 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.{{cite web | last=Salleh | first=Anna | title=Why Australia has so many pink lakes and why some of them are losing their colour| website= ABC News |series= ABC Science| publisher= Australian Broadcasting Corporation| date=4 January 2022 | url=https://www.abc.net.au/news/science/2022-01-05/pink-lakes-why-does-australia-have-so-many/100664354 | access-date=21 January 2022}}{{cite web | title=Here's the Real Reason Why Australia Has Bubblegum Pink Lakes | website=Discovery | date=24 December 2019 | url=https://www.discovery.com/science/Australia-Bubblegum-Pink-Lakes | access-date=22 January 2022}}{{cite web | title=Why is Pink Lake on Middle Island, off the coast of Esperance, pink? | website=Australia's Golden Outback | date=18 January 2021 | url=https://www.australiasgoldenoutback.com/whyispinklakehillierpink | access-date=22 January 2022 | others=Includes extract from Australian Geographic article. | archive-date=12 February 2022 | archive-url=https://web.archive.org/web/20220212134549/https://www.australiasgoldenoutback.com/whyispinklakehillierpink | url-status=dead }}{{cite web | last=Cassella | first=Carly | title=How an Australian lake turned bubble-gum pink | website=Australian Geographic | date=13 December 2016 | url=https://www.australiangeographic.com.au/topics/science-environment/2016/12/australias-pink-lakes/ | access-date=22 January 2022}} 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.

H. salinarum is polyploid{{cite journal |vauthors=Soppa J |title=Ploidy and gene conversion in Archaea |journal=Biochem. Soc. Trans. |volume=39 |issue=1 |pages=150–4 |year=2011 |pmid=21265763 |doi=10.1042/BST0390150 }} and highly resistant to ionizing radiation and desiccation, conditions that induce DNA double-strand breaks.{{cite journal |vauthors=Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J |title=Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation |journal=Extremophiles |volume=9 |issue=3 |pages=219–27 |year=2005 |pmid=15844015 |doi=10.1007/s00792-005-0437-4 |s2cid=8391234 |url=https://hal-mnhn.archives-ouvertes.fr/mnhn-02862359/file/2005_Kottemann_Kish_NRC1%20physiological%20response%20to%20desiccation%20and%20gamma%20radiation.pdf }} 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.{{cite journal |vauthors=DeVeaux LC, Müller JA, Smith J, Petrisko J, Wells DP, DasSarma S |title=Extremely radiation-resistant mutants of a halophilic archaeon with increased single-stranded DNA-binding protein (RPA) gene expression |journal=Radiat. Res. |volume=168 |issue=4 |pages=507–14 |year=2007 |pmid=17903038 |doi=10.1667/RR0935.1 |bibcode=2007RadR..168..507D |s2cid=22393850 |doi-access=free }}

Whole genome sequences are available for two strains of H. salinarum, NRC-1 and R1.{{cite journal | pmid = 18313895 | year = 2008 | last1 = Pfeiffer | first1 = F | title = Evolution in the laboratory: The genome of Halobacterium salinarum strain R1 compared to that of strain NRC-1 | journal = Genomics | volume = 91 | issue = 4 | pages = 335–46 | last2 = Schuster | first2 = S. C. | last3 = Broicher | first3 = A | last4 = Falb | first4 = M | last5 = Palm | first5 = P | last6 = Rodewald | first6 = K | last7 = Ruepp | first7 = A | last8 = Soppa | first8 = J | last9 = Tittor | first9 = J | last10 = Oesterhelt | first10 = D | doi = 10.1016/j.ygeno.2008.01.001 | doi-access = free }} 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. The large chromosome is very G-C rich (68%).{{cite journal | pmid = 13964964 | year = 1963 | last1 = Joshi | first1 = J. G. | title = The presence of two species of DNA in some halobacteria | journal = Journal of Molecular Biology | volume = 6 | pages = 34–8 | last2 = Guild | first2 = W. R. | last3 = Handler | first3 = P | doi=10.1016/s0022-2836(63)80079-0}} 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.

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,{{cite journal | pmid = 10672188 | year = 2000 | last1 = Peck | first1 = R. F. | title = Homologous gene knockout in the archaeon Halobacterium salinarum with ura3 as a counterselectable marker | journal = Molecular Microbiology | volume = 35 | issue = 3 | pages = 667–76 | last2 = Dassarma | first2 = S | last3 = Krebs | first3 = M. P. | doi=10.1046/j.1365-2958.2000.01739.x| doi-access = free }} so H. salinarum is an ideal candidate for the study of archaeal genetics and functional genomics.

Hydrogen production using H. salinarum coupled to a hydrogenase donor like E. coli are reported in literature.{{cite journal|last1=Brijesh Rajanandam|first1=K S|last2=Siva Kiran|first2=R R|title=Optimization of hydrogen production by Halobacterium salinarium coupled with E coli using milk plasma as fermentative substrate|journal=Journal of Biochemical Technology|date=2011|volume=3|issue=2|pages=242–244|url=http://www.jbiochemtech.com/index.php/jbt/article/viewFile/JBT321/pdf_9|issn=0974-2328}}

In the 1990s there were claims that DNA samples from Halobacteria from salt formations were millions of years old. Later analysis was unable to replicate the findings.{{cite journal | vauthors = Pääbo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, Kuch M, Krause J, Vigilant L, Hofreiter M | title = Genetic analyses from ancient DNA | journal = Annual Review of Genetics | volume = 38 | issue = 1 | pages = 645–79 | year = 2004 | pmid = 15568989 | doi = 10.1146/annurev.genet.37.110801.143214 | url = http://www.454genomics.net/downloads/news-events/geneticanalysisfromancientdna.pdf | url-status = dead | archive-url = https://web.archive.org/web/20081217110352/http://www.454genomics.net/downloads/news-events/geneticanalysisfromancientdna.pdf | archive-date = December 17, 2008 }}

Then in 2009 it was claimed that a sample of a close genetic relative of H. salinarum encapsulated in salt allowed for the recovery of ancient DNA fragments estimated at 121 million years old.{{cite web

| url = http://www.nbcnews.com/id/34467577

| archive-url = https://web.archive.org/web/20200923230747/http://www.nbcnews.com/id/34467577

| url-status = dead

| archive-date = September 23, 2020

| title = World's oldest known DNA discovered

| access-date = 3 September 2010

| author = Reilly, Michael

| author2 = The Discovery Channel

}} 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.{{cite journal

|doi=10.1111/j.1472-4669.2009.00218.x

|author=Park, J. S.

|author2=Vreeland, R. H.

|author3=Cho, B. C.

|author4=Lowenstein, T. K.

|author5=Timofeeff, M. N.

|author6=Rosenweig, W. D.

|name-list-style=amp

|title=Haloarchaeal diversity in 23, 121 and 419 MYA salts

|journal=Geobiology

|volume=7

|issue=5

|pages=515–23

|date=December 2009

|pmid=19849725

}} 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 also claimed to discover a halophile estimated at 250 million years old in New Mexico.{{cite journal |doi=10.1007/s00792-005-0474-z |author1=Vreeland, H |author2=Rosenzweig, W D |author3=Lowenstein, T |author4=Satterfield, C |author5=Ventosa, A |title=Fatty acid and DNA analyses of Permian bacteria isolated from ancient salt crystals reveal differences from their modern relatives|journal=Extremophiles|volume=10|issue=1|pages=71–8|date=December 2006 |pmid=16133658|s2cid=25102006 }} However, his findings date the crystal surrounding the bacteria, and DNA analysis suggests the bacteria themselves are likely to be less ancient.{{cite journal|title=The Permian Bacterium that Isn't |journal=Molecular Biology and Evolution |volume=18 |issue=6 |pages=1143–1146 |publisher=Oxford Journals |date=2001-02-15 |doi=10.1093/oxfordjournals.molbev.a003887 |pmid=11371604 |last1=Graur |first1=Dan |last2=Pupko |first2=Tal |doi-access=free }}

In 2022, a study in Nature reported that two-million year old preserved genetic material from many species was found in Greenland, and these sequences are currently considered the oldest confirmed DNA discovered, of any species.{{cite news | vauthors = Zimmer C |authorlink=Carl Zimmer |title=Oldest Known DNA Offers Glimpse of a Once-Lush Arctic - In Greenland's permafrost, scientists discovered two-million-year-old genetic material from scores of plant and animal species, including mastodons, geese, lemmings and ants. |url=https://www.nytimes.com/2022/12/07/science/oldest-dna-greenland-species.html |date=7 December 2022 |work=The New York Times |access-date=7 December 2022 }}{{cite journal | vauthors = Kjær KH, Winther Pedersen M, De Sanctis B, De Cahsan B, Korneliussen TS, Michelsen CS, Sand KK, Jelavić S, Ruter AH, Schmidt AM, Kjeldsen KK, Tesakov AS, Snowball I, Gosse JC, Alsos IG, Wang Y, Dockter C, Rasmussen M, Jørgensen ME, Skadhauge B, Prohaska A, Kristensen JÅ, Bjerager M, Allentoft ME, Coissac E, Rouillard A, Simakova A, Fernandez-Guerra A, Bowler C, Macias-Fauria M, Vinner L, Welch JJ, Hidy AJ, Sikora M, Collins MJ, Durbin R, Larsen NK, Willerslev E | title = A 2-million-year-old ecosystem in Greenland uncovered by environmental DNA | journal = Nature | volume = 612 | issue = 7939 | pages = 283–291 | date = December 2022 | pmid = 36477129 | pmc = 9729109 | doi = 10.1038/s41586-022-05453-y | bibcode = 2022Natur.612..283K }}

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• {{cite journal|last1=Horia|first1=Todor|last2=Dulmage|first2=Keely|last3=Gillum|first3=Nicholas|last4=Bain|first4=James|last5=Muehlbauer|first5=Michael|last6=Schmid|first6=Amy|title=A transcription factor links growth rate and metabolism in the hypersaline adapted archaeon Halobacterium salinarum|journal=Molecular Microbiology|date= 2014|volume=93|issue=6|pages=1172–1182|doi=10.1111/mmi.12726|pmid=25060603|doi-access=free}}
• {{cite journal|last1=Kahaki|first1=Fatemeh Abarghooi|last2=Babaeipour|first2=Valiollah|last3=Memari|first3=Hamid Rajabi|last4=Mofid|first4=Mohammad Reza|title=High Overexpression and Purification of Optimized Bacterio-Opsin from Halobacterium Salinarum R1 in E-coli|journal=Applied Biochemistry and Biotechnology|date= 2014|volume=174|issue=4|pages=1558–1571|doi=10.1007/s12010-014-1137-2|pmid=25123363|s2cid=7403305}}

• [http://bacdive.dsmz.de/index.php?search=5912&submit=Search Type strain of Halobacterium salinarum at BacDive - the Bacterial Diversity Metadatabase]

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Category:Halobacteria

Category:Archaea described in 1922

Category:Halophiles