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GFAJ-1

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GFAJ-1
Magnified cells of bacterium GFAJ-1 grown in medium containing arsenate
Scientific classification
Domain:
Bacteria
Phylum:
Proteobacteria
Class:
Gammaproteobacteria
Order:
Oceanospirillales
Family:
Halomonadaceae

GFAJ-1 is a strain of rod-shaped bacterium in the family Halomonadaceae. The extremophile was isolated from the hypersaline and alkaline Mono Lake in eastern California, and reported as new to science by a research team led by NASA astrobiologist Felisa Wolfe-Simon in a 2010 Science journal publication.[1] According to the authors, the microbe, when starved of phosphorus, is capable of substituting arsenic for a small percentage of its phosphorus and sustain its growth.[2][3] Immediately after publication, other microbiologists and biochemists expressed doubt about this hypothesis, and the claim that this bacterium uses arsenic instead of phosphorus in its metabolism is robustly debated in the scientific community.

Discovery

Tufa formations along the shore of Mono Lake

The GFAJ-1 bacterium was discovered by geomicrobiologist Felisa Wolfe-Simon, a NASA astrobiology fellow in residence at the US Geological Survey in Menlo Park, California.[4] GFAJ stands for "Give Felisa a Job".[5] The organism was isolated and cultured beginning in 2009 from samples she and her colleagues collected from sediments at the bottom of Mono Lake, California, U.S.A.[6] Mono Lake is hypersaline (about 90 grams/liter) and highly alkaline (pH 9.8).[7] It also has one of the highest natural concentrations of arsenic in the world (200 μM).[1] The discovery was widely publicized on 2 December 2010.[2]

Taxonomy and phylogeny

Escherichia coli strain O157:H7

Halomonas alkaliphila

Halomonas venusta strain NBSL13

GFAJ-1

Halomonas sp. GTW

Halomonas sp. G27

Halomonas sp. DH77

Halomonas sp. mp3

Halomonas sp. IB-O18

Halomonas sp. ML-185

Phylogeny of GFAJ-1 and closely related bacteria based on ribosomal DNA sequences.[8]

Molecular analysis based on 16S rRNA sequences shows GFAJ-1 to be closely related to other moderate halophile ("salt-loving") bacteria of the family Halomonadaceae. Although the authors produced a cladogram in which the strain is nested among members of Halomonas, including H. alkaliphila and H. venusta,[8] they did not explicitly assign the strain to that genus.[1][6] Many bacteria are known to be able to tolerate high levels of arsenic, and to have a proclivity to take it up into their cells.[1][9] However, GFAJ-1 has now been proposed to go a step further; when starved of phosphorus, it can instead incorporate arsenic into its metabolites and macromolecules and continue growing.[6]

Species/strain

In the Science journal article, GFAJ-1 is referred to as a strain of Halomonadaceae and not as a new species.[1] In fact, the International Code of Nomenclature of Bacteria (a body which governs the taxonomy of bacteria) has guidelines outlined in the Bacteriological Code which require certain conditions to be met for a new species to be accepted, such as evidence of a new species (e.g., less that 97% 16S rRNA sequence identity from other species,[10]) deposition of the strain in at least two microbiological repositories and proposed name in italics followed by sp. nov. (and gen. nov. if it is a novel genus according to the descriptions of that clade);[11][12] in the instance of the GFAJ-1 strain this is not met.[1] When a strain cannot be assigned to a species (novel, insufficient data, author choice) it is labeled as the genus name followed by "sp." (i.e., undetermined species of that genus) (both in italics) and the strain name (in roman type). If the conclusion of some critics that the strain is a member of Halomonas genus,[6] the strain can be referred to as Halomonas sp. GFAJ-1. Strains closely related to GFAJ-1 include Halomonas sp. GTW and Halomonas sp. G27, neither of which were identified to be a valid species.[13][14]

Biochemistry

Scanning electron micrograph of GFAJ-1 cells grown in defined minimal medium supplemented with 1.5 mM phosphate

A phosphorus-free growth medium (which actually contained 3.1 ± 0.3 μM of residual phosphate, from impurities in reagents) was used to culture the bacteria in a regime of increasing exposure to arsenate; the initial level of 0.1 mM was eventually ramped up to 40 mM. Alternative media used for comparative experiments contained either high levels of phosphate (1.5 mM) with no arsenate, or had neither added phosphate nor added arsenate. It was observed that GFAJ-1 could grow through many doublings in cell numbers when cultured in either phosphate or arsenate media, but could not grow when placed in a medium of a similar composition to which neither phosphate nor arsenate was added.[1] The phosphorus content of the arsenic-fed, phosphorus-starved bacteria (as measured by ICP-MS) was only 0.019 (± 0.001) % by dry weight, one thirtieth of that when grown in phosphate, and about one hundredth that of most bacteria. This phosphorus content was also only about one tenth of the cells' arsenic content (0.19 ± 0.25 % by dry weight).[1] Other data from the same study obtained with nano-SIMS does however suggest a ~75-fold excess of phosphate (P) over arsenic (As) when expressed as P:C and As:C ratios, even in cells grown with arsenate and no added phosphate.[8] When cultured in the arsenate solution, GFAJ-1 only grew 60% as fast as it did in phosphate solution.[2] The phosphate-starved bacteria had an intracellular volume 1.5 times normal; the greater volume appeared to be associated with the appearance of large "vacuole-like regions".[1]

When the researchers added isotope-labeled arsenate to the solution to track its distribution, they found that arsenic was present in the cellular fractions containing the bacteria's proteins, lipids and metabolites such as ATP, as well as its DNA and RNA.[2] Nucleic acids from stationary phase cells starved of phosphorus were concentrated via five extractions (one with phenol, three with phenol-chloroform and one with chloroform extraction solvent), followed by ethanol precipitation. Although direct evidence of the incorporation of arsenic into biomolecules is still lacking, radioactivity measurements suggested that approximately one-tenth (11.0 ± 0.1 %) of the arsenic absorbed by these bacteria ended up in the fraction that contained the nucleic acids (DNA and RNA) and all other co-precipitated compounds not extracted by the previous treatments.[1] A comparable control experiment with isotope-labeled phosphate was not performed.

Arsenate ester stability

Structure of poly-β-hydroxybutyrate

Arsenate esters, such as those that would be present in DNA, are generally expected to be orders of magnitude less stable to hydrolysis than corresponding phosphate esters.[15] dAMAs, the structural arsenic analog of the DNA building block dAMP, has a half-life of 40 minutes in water at neutral pH.[16] The authors speculate that the bacteria may stabilize arsenate esters to a degree by using poly-β-hydroxybutyrate (which has been found to be elevated in "vacuole-like regions" of related species of the genus Halomonas) or other means to lower the effective concentration of water.[1][6] Polyhydroxybutyrates are used by many bacteria for energy and carbon storage under conditions when growth is limited by elements other than carbon, and typically appear as large waxy granules closely resembling the "vacuole-like regions" seen in GFAJ-1 cells.[17] The authors present no mechanism by which insoluble polyhydroxybutyrate may lower the effective concentration of water in the cytoplasm sufficiently to stabilize arsenate esters. Although all halophiles must reduce the water activity of their cytoplasm by some means to avoid desiccation,[18] the cytoplasm always remains an aqueous environment.

Possible implications

The discovery of a microorganism that allegedly can use arsenic to build some of its cellular components has implications in the area of astrobiology,[19] as this could suggest that life may form in the absence of large amounts of available phosphorus, thus increasing the probability of finding life elsewhere in the universe.[3][6] If the study is correct, this finding may support the long-standing hypothesis that life on other planets may have a chemical makeup differing from that of known organisms in fundamental ways, and could help in the search for extraterrestrial life.[2][3][20] It has also been speculated that use of arsenic in place of phosphorus on Earth may date back to the origin of life, which may have occurred in arsenic-rich hydrothermal vent environments.[21][22]

Criticism

NASA's announcement of a news conference "that will impact the search for evidence of extraterrestrial life" was criticized as sensationalistic and misleading; an editorial in New Scientist commented "although the discovery of alien life, if it ever happens, would be one of the biggest stories imaginable, this was light-years from that."[23][24]

In addition, many experts who have evaluated the paper have concluded that the reported studies do not provide enough evidence to support the claims made by the authors.[25] In an online article on Slate, science writer Carl Zimmer discussed the skepticism of several scientists: "I reached out to a dozen experts ... Almost unanimously, they think the NASA scientists have failed to make their case."[26]

Chemist Steven A. Benner has expressed doubts that arsenate has replaced phosphate in the DNA of this organism. He suggested that the trace contaminants in the growth medium used by Wolfe-Simon in her laboratory cultures are sufficient to supply the phosphorus needed for the cells' DNA. He believes that it is more likely that arsenic is being sequestered elsewhere in the cells.[2][6] University of British Columbia microbiologist Rosemary Redfield said that the paper "doesn't present any convincing evidence that arsenic has been incorporated into DNA or any other biological molecule," and suggests that the experiments lacked the washing steps and controls necessary to properly validate their conclusions.[27][28] Harvard microbiologist Alex Bradley says that arsenic-containing DNA would be so unstable in water it could not have survived the analysis procedure.[26][29]

On 8 December 2010, Science journal published a response by Wolfe-Simon, in which she states that criticism of the research was expected. In response, a "Frequently Asked Questions" page to improve understanding of the work was published on 16 December 2010.[30] They plan to deposit the GFAJ-1 strain in the ATCC and DSMZ culture collections to allow widespread distribution. Science journal will also be making the article freely available for two weeks.[31]

See also

References

  1. ^ a b c d e f g h i j k Wolfe-Simon, Felisa (2 December 2010). "A bacterium that can grow by using arsenic instead of phosphorus" (PDF). Science. doi:10.1126/science.1197258. PMID 21127214. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  2. ^ a b c d e f Katsnelson, Alla (2 December 2010). "Arsenic-eating microbe may redefine chemistry of life". Nature News. doi:10.1038/news.2010.645. Retrieved 2010-12-02.
  3. ^ a b c Palmer, Jason (2 December 2010). "Arsenic-loving bacteria may help in hunt for alien life". BBC News. doi:10.1038/news.2010.645. Retrieved 2010-12-02.
  4. ^ Bortman, Henry (5 October 2009). "Searching for Alien Life, on Earth". Astrobiology Magazine (NASA). Retrieved 2010-12-02. {{cite web}}: External link in |publisher= (help)
  5. ^ Davies, Paul (4 December 2010). "The 'Give Me a Job' Microbe". Wall Street Journal. Retrieved 2010-12-05.
  6. ^ a b c d e f g Bortman, Henry (2 December 2010). "Thriving on arsenic". Astrobiology Magazine (NASA). Retrieved 2010-12-04. {{cite news}}: External link in |publisher= (help)
  7. ^ Oremland, Ronald S.; Stolz, John F. (9 May 2003). "The ecology of arsenic" (PDF). Science. 300 (5621): 939–944. doi:10.1126/science.1081903. PMID 12738852.
  8. ^ a b c Wolfe-Simon, Felisa; et al. (2 December 2010). "A bacterium that can grow by using arsenic instead of phosphorus: Supporting online material" (PDF). Science. doi:10.1126/science.1197258. {{cite journal}}: Explicit use of et al. in: |author= (help)
  9. ^ Stolz, John F.; Basu, Partha; Santini, Joanne M.; Oremland, Ronald S. (2006). "Arsenic and selenium in microbial metabolism". Annual Review of Microbiology. 60: 107–30. doi:10.1146/annurev.micro.60.080805.142053. PMID 16704340. {{cite journal}}: External link in |journal= (help)
  10. ^ Stackebrandt, Erko; Ebers, Jonas (2006). "Taxonomic parameters revisited: tarnished gold standards" (PDF). Microbiology Today. 33 (4): 152–155.
  11. ^ Sneath, P.H.A (1992). Lapage S.P.; Sneath, P.H.A.; Lessel, E.F.; Skerman, V.B.D.; Seeliger, H.P.R.; Clark, W.A. (ed.). International Code of Nomenclature of Bacteria. Washington, D.C.: American Society for Microbiology. ISBN 1-55581-039-X. PMID 21089234.{{cite book}}: CS1 maint: multiple names: editors list (link)
  12. ^ Euzéby J.P. (2010). "Introduction". List of Prokaryotic names with Standing in Nomenclature. Retrieved 2010-12-11.
  13. ^ Guo, Jianbo; Zhou, Jiti; Wang, Dong; Tian, Cunping; Wang, Ping; Uddin, M. Salah (2008). "A novel moderately halophilic bacterium for decolorizing azo dye under high salt condition". Biodegradation. 19 (1): 15–19. doi:10.1007/s10532-007-9110-1.
  14. ^ Kiesel, B.; Müller, R.H.; Kleinsteuber, R. (2007). "Adaptative potential of alkaliphilic bacteria towards chloroaromatic substrates assessed by a gfp-tagged 2,4-D degradation plasmid". Engineering in Life Sciences. 7 (4): 361–372. doi:10.1002/elsc.200720200.
  15. ^ Westheimer, F.H. (6 June 1987). "Why nature chose phosphates" (PDF). Science. 235 (4793): 1173–1178 (see pp. 1175–1176). doi:10.1126/science.2434996.
  16. ^ Lagunas, Rosario; Pestana, David; Diez-Masa, Jose C. (1984). "Arsenic mononucleotides. Separation by high-performance liquid chromatography and identification with myokinase and adenylate deaminase". Biochemistry. 23 (5): 955–960. doi:10.1021/bi00300a024. PMID 6324859.
  17. ^ Quillaguamána, Jorge (January 2006). "Poly(β-hydroxybutyrate) production by a moderate halophile, Halomonas boliviensis LC1". Enzyme and Microbial Technology. 38 (1–2). Elsevier Inc.: 148–154. doi:10.1016/j.enzmictec.2005.05.013. PMID 15960675. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  18. ^ Oren, Aharon (June 1999). "Bioenergetic aspects of halophilism". Microbiology and Molecular Biology Reviews. 63 (2). American Society for Microbiology: 334–348. ISSN 1092-2172. PMID 10357854.
  19. ^ Cohn, Vicki (7 December 2010). "Field of astrobiology more vital than ever". Mary Ann Lieber Inc. Genetic Engineering News. Retrieved 2010-12-08. {{cite news}}: External link in |work= (help)
  20. ^ Harvey, Mike (4 March 2010). "Could the Mono Lake arsenic prove there is a shadow biosphere?". The Times. Retrieved 2010-12-02.
  21. ^ Reilly, Michael (26 April 2008). "Early life could have relied on 'arsenic DNA'". New Scientist. 198 (2653): 10. doi:10.1016/S0262-4079(08)61007-6.
  22. ^ Pennisi, Elizabeth (3 December 2010). "What poison? Bacterium uses arsenic to build DNA and other molecules". Science. 330 (6009). AAAS: 1302. doi:10.1126/science.330.6009.1302.
  23. ^ Opinion (8 December 2010). "Curb your enthusiasm for aliens, NASA". New Scientist (2790). New Scientist: 5. Retrieved 2010-12-09. {{cite journal}}: External link in |work= (help)
  24. ^ MEDIA ADVISORY : M10-167, NASA Sets News Conference on Astrobiology Discovery; Science Journal Has Embargoed Details Until 2 p.m. EST On Dec. 2 Nov. 29, 2010
  25. ^ Carmen Drahl (2010). "Arsenic Bacteria Breed Backlash". Chemical & Engineering News. 88 (50): 7.
  26. ^ a b Zimmer, Carl (7 December 2010). "Scientists see fatal flaws in the NASA study of arsenic-based life". Slate. Retrieved 2010-12-07.
  27. ^ Redfield, Rosemary (4 December 2010). "Arsenic-associated bacteria (NASA's claims)". RR Research blog. Retrieved 2010-12-04. {{cite web}}: External link in |work= (help)
  28. ^ Redfield, Rosemary (8 December 2010). "My Letter to Science". RR Research blog. Retrieved 2010-12-09. {{cite web}}: External link in |work= (help)
  29. ^ Bradley, Alex (5 December 2010). "Arsenate-based DNA: a big idea with big holes". We, Beasties blog. Retrieved 2010-12-09. {{cite web}}: External link in |work= (help)
  30. ^ Wolfe-Simon, Felisa (December 16, 2010). "Response to Questions Concerning the Science Article," (PDF). Retrieved 2010-12-17.
  31. ^ Pennisi, Elizabeth (8 December 2010). "Author of controversial arsenic paper speaks". ScienceInsider. Science. Retrieved 2010-12-11. {{cite web}}: External link in |work= (help)
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