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Deinococcus radiodurans

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Deinococcus radiodurans
A tetrad of D. radiodurans
Scientific classification
Kingdom:
Bacteria
Phylum:
Deinococcus-Thermus
Order:
Deinococcales
Genus:
Deinococcus
Species:
D. radiodurans
Binomial name
Deinococcus radiodurans
Brooks & Murray, 1981

Deinococcus radiodurans is an extremophilic bacterium, one of the most radioresistant organisms known. It can survive cold, dehydration, vacuum, and acid, and is therefore known as a polyextremophile and has been listed as the world's toughest bacterium in The Guinness Book Of World Records.[1]

Name and classification

The name Deinococcus radiodurans derives from the Ancient Greek δεινός (deinos) and κόκκος (kokkos) meaning "terrible grain/berry" and the Latin radius and durare, meaning "radiation surviving". The species was formerly called Micrococcus radiodurans. As a consequence of its hardiness, it has been nicknamed Conan the Bacterium.[2]

Initially, it was placed in the genus Micrococcus. After evaluation of ribosomal RNA sequences and other evidence, it was placed in its own genus Deinococcus, which is closely related to the genus Thermus of heat-resistant bacteria; the group consisting of the two is accordingly known as Deinococcus-Thermus.[3]

Deinococcus is the only genus in the order Deinococcales. D. radiodurans is the type species of this genus, and the best studied member. All known members of the genus are radioresistant: D. proteolyticus, D. radiopugnans, D. radiophilus, D. grandis, D. indicus, D. frigens, D. saxicola, D. marmoris, D. deserti,[4] D. geothermalis and D. murrayi; the latter two are also thermophilic.[5]

History

D. radiodurans was discovered in 1956 by Arthur W. Anderson at the Oregon Agricultural Experiment Station in Corvallis, Oregon.[6] Experiments were being performed to determine if canned food could be sterilized using high doses of gamma radiation. A tin of meat was exposed to a dose of radiation that was thought to kill all known forms of life, but the meat subsequently spoiled, and D. radiodurans was isolated.

The complete DNA sequence of D. radiodurans was published in 1999 by TIGR. A detailed annotation and analysis of the genome appeared in 2001.[3] The sequenced strain was ATCC BAA-816.

Deinococcus radiodurans has a unique quality in which it can repair both single- and double-stranded DNA. When a damage is apparent to the cell, it brings it into a compartmental ring-like structure, where the DNA is repaired and then is able to fuse the nucleoids from the outside of the compartment with the damaged DNA.[7]

Description

D. radiodurans is a rather large, spherical bacterium, with a diameter of 1.5 to 3.5 µm. Four cells normally stick together, forming a tetrad. The bacteria are easily cultured and do not appear to cause disease.[3] Colonies are smooth, convex, and pink to red in color. The cells stain Gram positive, although its cell envelope is unusual and is reminiscent of the cell walls of Gram negative bacteria.[8]

D. radiodurans does not form endospores and is nonmotile. It is an obligate aerobic chemoorganoheterotroph, i.e., it uses oxygen to derive energy from organic compounds in its environment. It is often found in habitats rich in organic materials, such as soil, feces, meat, or sewage, but has also been isolated from dried foods, room dust, medical instruments and textiles.[8]

It is extremely resistant to ionizing radiation, ultraviolet light, desiccation, and oxidizing and electrophilic agents.[9]

Its genome consists of two circular chromosomes, one 2.65 million base pairs long and the other 412,000 base pairs long, as well as a megaplasmid of 177,000 base pairs and a plasmid of 46,000 base pairs. It has about 3,195 genes. In its stationary phase, each bacterial cell contains four copies of this genome; when rapidly multiplying, each bacterium contains 8-10 copies of the genome.

Ionizing radiation resistance

D. radiodurans is capable of withstanding an acute dose of 5,000 Gy (500,000 rad) of ionizing radiation with almost no loss of viability, and an acute dose of 15,000 Gy with 37% viability.[10][11][12] A dose of 5,000 Gy is estimated to introduce several hundred double-strand breaks (DSBs) into the organism's DNA (~0.005 DSB/Gy/Mbp (haploid genome)). For comparison, a chest X-ray or Apollo mission involves about 1 mGy, 5 Gy can kill a human, 200-800 Gy will kill E. coli, and over 4,000 Gy will kill the radiation-resistant tardigrade.

Several bacteria of comparable radioresistance are now known, including some species of the genus Chroococcidiopsis (phylum cyanobacteria) and some species of Rubrobacter (phylum actinobacteria); among the archaea, the species Thermococcus gammatolerans shows comparable radioresistance.[5] Deinococcus radiodurans also has a unique ability to repair damaged DNA. It isolates the damaged segments in a controlled area and repairs it. This bacteria can also repair many small fragments from an entire chromosome.[13]

Ionizing radiation resistance mechanisms

Deinococcus accomplishes its resistance to radiation by having multiple copies of its genome and rapid DNA repair mechanisms. It usually repairs breaks in its chromosomes within 12–24 hours through a 2-step process. First, D. radiodurans reconnects some chromosome fragments through a process called single-stranded annealing. In the second step, multiple proteins mend double-strand breaks through homologous recombination. This process does not introduce any more mutations than a normal round of replication would.

A persistent question regarding D. radiodurans is how such a high degree of radioresistance could evolve. Natural background radiation levels are very low—in most places, on the order of 0.4 mGy per year, and the highest known background radiation, near Ramsar, Iran is only 260 mGy per year. With naturally occurring background radiation levels so low, organisms evolving mechanisms specifically to ward off the effects of high radiation are unlikely.

Valerie Mattimore of Louisiana State University has suggested the radioresistance of D. radiodurans is simply a side effect of a mechanism for dealing with prolonged cellular desiccation (dryness). To support this hypothesis, she performed an experiment in which she demonstrated that mutant strains of D. radiodurans which are highly susceptible to damage from ionizing radiation are also highly susceptible to damage from prolonged desiccation, while the wild-type strain is resistant to both.[14] In addition to DNA repair, D. radiodurans use LEA proteins (Late Embryogenesis Abundant proteins)[15] expression to protect against desiccation.[16]

Scanning electron microscopy analysis has shown that DNA in D. radiodurans is organized into tightly packed toroids, which may facilitate DNA repair.[17]

A team of Croatian and French researchers led by Miroslav Radman have bombarded D. radiodurans to study the mechanism of DNA repair. At least two copies of the genome, with random DNA breaks, can form DNA fragments through annealing. Partially overlapping fragments are then used for synthesis of homologous regions through a moving D-loop that can continue extension until they find complementary partner strands. In the final step, there is crossover by means of RecA-dependent homologous recombination.[18]

D. radiodurans is capable of genetic transformation, a process by which DNA derived from one cell can be taken up by another cell and integrated into the recipient genome by homologous recombination.[19] When DNA damages (e.g. pyrimidine dimers) are introduced into donor DNA by UV irradiation, the recipient cells efficiently repair the damages in the transforming DNA as they do in cellular DNA when the cells themselves are irradiated.

Michael Daly has suggested the bacterium uses manganese complexes as antioxidants to protect itself against radiation damage.[20] In 2007 his team showed that high intracellular levels of manganese(II) in D. radiodurans protect proteins from being oxidized by radiation, and proposed the idea that "protein, rather than DNA, is the principal target of the biological action of [ionizing radiation] in sensitive bacteria, and extreme resistance in Mn-accumulating bacteria is based on protein protection".[21]

A team of Russian and American scientists proposed that the radioresistance of D. radiodurans had a Martian origin. Evolution of the microorganism could have taken place on the Martian surface until it was delivered to Earth on a meteorite.[22] However, apart from its resistance to radiation, Deinococcus is genetically and biochemically very similar to other terrestrial life forms, arguing against an extraterrestrial origin.

In 2009, nitric oxide was reported to play an important role in the bacteria's recovery from radiation exposure: the gas is required for division and proliferation after DNA damage has been repaired. A gene was described that increases nitric oxide production after UV radiation, and in the absence of this gene, the bacteria were still able to repair DNA damage, but would not grow.[23]

Applications

Deinococcus has been genetically engineered for use in bioremediation to consume and digest solvents and heavy metals, even in a highly radioactive site. For example, the bacterial mercuric reductase gene has been cloned from Escherichia coli into Deinococcus to detoxify the ionic mercury residue frequently found in radioactive waste generated from nuclear weapons manufacture.[24] Those researchers developed a strain of Deinococcus that could detoxify both mercury and toluene in mixed radioactive wastes.

The Craig Venter Institute has used a system derived from the rapid DNA repair mechanisms of D. radiodurans to assemble synthetic DNA fragments into chromosomes, with the ultimate goal of producing a synthetic organism they call Mycoplasma laboratorium.[25]

In 2003, U.S. scientists demonstrated D. radiodurans could be used as a means of information storage that might survive a nuclear catastrophe. They translated the song "It's a Small World" into a series of DNA segments 150 base pairs long, inserted these into the bacteria, and were able to retrieve them without errors 100 bacterial generations later. However, since only a small portion of the information can be stored in DNA of D. radiodurans, several species had to be created, each holding a different part of the song and species needed to be kept segregated over time. If species are evolving together after a number of generations certain species will emerge dominant and others will become extinct and parts of the encoded message which were stored in extinct species will be lost.[26]

See also

References

  1. ^ Sarah DeWeerdt. "The World's Toughest Bacterium".
  2. ^ Huyghe, Patrick (July/August 1998). "Conan the Bacterium" (PDF). The Sciences. New York Academy of Sciences: 16–19. {{cite journal}}: Check date values in: |date= (help)
  3. ^ a b c Makarova, K S (March 2001). "Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics". Microbiology and molecular biology reviews : MMBR. 65 (1): 44–79. doi:10.1128/MMBR.65.1.44-79.2001. PMC 99018. PMID 11238985. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  4. ^ de Groot A, Chapon V, Servant P, Christen R, Saux MF, Sommer S, Heulin T (November 2005). "Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert". Int J Syst Evol Microbiol. 55 (Pt 6): 2441–2446. doi:10.1099/ijs.0.63717-0. PMID 16280508.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  5. ^ a b Cox, Michael M (November 2005). "Deinococcus radiodurans — the consummate survivor" (PDF). Nature reviews. Microbiology. 3 (11): 882–92. doi:10.1038/nrmicro1264. PMID 16261171. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  6. ^ Anderson, A W (1956). "Studies on a radio-resistant micrococcus. I. Isolation, morphology, cultural characteristics, and resistance to gamma radiation". Food Technol. 10 (1): 575–577. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  7. ^ Clark, D.P, Dunlap, P.V., Madigan, M.T., Martinko, J.M. Brock Biology of Microorganisms. San Francisco: Pearson; 2009. 481 p
  8. ^ a b Battista, J R (1997). "Against all odds: the survival strategies of Deinococcus radiodurans" (PDF). Annual review of microbiology. 51: 203–24. doi:10.1146/annurev.micro.51.1.203. PMID 9343349.
  9. ^ Slade D, Radman M. (2011). Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75(1):133-91. doi: 10.1128/MMBR.00015-10. Review. PMID 21372322
  10. ^ Moseley BEB, Mattingly A (1971). "Repair of irradiated transforming deoxyribonu- cleic acid in wild type and a radiation- sensitive mutant of Micrococcus radiodu- rans". J. Bacteriol. 105 (3): 976–83. PMC 248526. PMID 4929286.
  11. ^ Murray RGE. 1992. The family Deino- coccaceae. In The Prokaryotes, ed. A Ballows, HG Truper, M Dworkin, W Harder, KH Schleifer 4:3732–44. New York: Springer-Verlag
  12. ^ Ito H, Watanabe H, Takeshia M, Iizuka H (1983). "Isolation and identification of radiation-resistant cocci belonging to the genus Deinococcus from sewage sludges and animal feeds. Agric". Biol. Chem. 47: 1239–47.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  13. ^ Clark, D.P., Dunlap, P.V., Madigan, M.T., Martinko, J.M. Brock Biology of Microorganisms. San Francisco: Pearson. 2009. 281 p.
  14. ^ Mattimore V, Battista JR (1 February 1996). "Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation". Journal of Bacteriology. 178 (3): 633–637. PMC 177705. PMID 8550493.
  15. ^ Goyal K, Walton LJ, Tunnacliffe A (2005). "LEA proteins prevent protein aggregation due to water stress". Biochemical Journal. 388 (Pt 1): 151–157. doi:10.1042/BJ20041931. PMC 1186703. PMID 15631617.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  16. ^ Battista JR, Park MJ, McLemore AE (2001). "Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation". Cryobiology. 43 (2): 133–139. doi:10.1006/cryo.2001.2357. PMID 11846468.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  17. ^ Levin-Zaidman S, Englander J, Shimoni E, Sharma AK, Minton KW, Minsky A (2003). "Ringlike structure of the Deinococcus radiodurans genome: a key to radioresistance?". Science. 299 (5604): 254–256. Bibcode:2003Sci...299..254L. doi:10.1126/science.1077865. PMID 12522252.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  18. ^ Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, Petranovic M, Lindner AB, Radman M (2006). "Reassembly of shattered chromosomes in Deinococcus radiodurans" (PDF). Nature. 443 (7111): 569–573. Bibcode:2006Natur.443..569Z. doi:10.1038/nature05160. PMID 17006450.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  19. ^ Moseley BE, Setlow JK. (1968). Transformation in Micrococcus radiodurans and the ultraviolet sensitivity of its transforming DNA. Proc Natl Acad Sci U S A 61(1):176-183. PMID 5303325 PMCID: PMC285920
  20. ^ Pearson, Helen (30 September 2004). "Secret of radiation-proof bugs proposed" (PDF). news@nature.com. Archived from the original (PDF) on 2006-01-04. Retrieved 2006-06-19.
  21. ^ Daly, Michael J. (2007-04-01). "Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance". PLoS Biology. 5 (4): e92 EP –. doi:10.1371/journal.pbio.0050092. PMC 1828145. PMID 17373858. {{cite journal}}: |access-date= requires |url= (help); Unknown parameter |coauthors= ignored (|author= suggested) (help)CS1 maint: unflagged free DOI (link)
  22. ^ Pavlov AK, Kalinin VL, Konstantinov AN, Shelegedin VN, Pavlov AA (2006). "Was Earth ever infected by martian biota? Clues from radioresistant bacteria" (PDF). Astrobiology. 6 (6): 911–918. Bibcode:2006AsBio...6..911P. doi:10.1089/ast.2006.6.911. PMID 17155889.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  23. ^ Krishna Ramanujan (October 19, 2009). "Research reveals key to world's toughest organism". Physorg.com.
  24. ^ Brim H, McFarlan SC, Fredrickson JK, Minton KW, Zhai M, Wackett LP, Daly MJ (2000). "Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments" (PDF). Nature Biotechnology. 18 (1): 85–90. doi:10.1038/71986. PMID 10625398.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  25. ^ Craig Venter's TED talk (February 2005) mentions D. radiodurans as the ultimate genome assembly machine
  26. ^ McDowell, Natasha (2003-01-08). "Data stored in multiplying bacteria". New Scientist. Retrieved 2011-04-01.
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