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GFAJ-1

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

GFAJ-1 (GFAJ stands for "Give Felisa a Job" [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 publication. According to the authors, the microbe, when starved of phosphorus, is capable of incorporating the element arsenic in its proteins, lipids and metabolites such as ATP, as well as its DNA and RNA, but direct evidence for this is still lacking.[2][3] The mechanism by which, or indeed if, arsenic is integrated into the cell's biomolecular structures is not known, and the results have been met with skepticism by some scientists. The discovery of the microbe lends weight to the long-standing idea that extraterrestrial life could have a fundamentally different chemical makeup from life on Earth.[3][4]

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 Geologic Survey in Menlo Park, California.[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.[4] Mono Lake is hypersaline and highly alkaline. It also has one of the highest natural concentrations of arsenic in the world (200 μM).[6] 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.[7]

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 strain appears to be closely related to members of Halomonas, including H. alkaliphila and H. venusta, the authors did not explicitly assign the strain to that genus.[4][6] Many of these bacteria are known to be able to tolerate high levels of arsenic, and to have a proclivity to take it up into their cells.[6] 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.[4]

Biochemistry

Magnified cells of bacterium GFAJ-1 grown on phosphorus

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 neither phosphate nor arsenate. It was observed that GFAJ-1 could grow through many doublings in cell concentration when cultured in either phosphate or arsenate media, but could not grow when placed in medium that lacked both phosphate and arsenate.[6] 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).[6] Other data from the same study does however suggest a ~75-fold excess of P over As when expressed as P:C and As:C ratios, even in cells grown with arsenate and no added phosphate.[6] 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".[6]

When the researchers added radiolabeled 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 and all other co-precipitated compounds not extracted by the previous treatments.[6] A comparable control experiment with radiolabeled phosphate was not performed.

Arsenate ester stability

Structure of poly-β-hydroxybutyrate

Arsenate esters, such as those that would be present in arsenate DNA, are generally expected to be orders of magnitude less stable to hydrolysis than corresponding phosphate esters.[8] 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.[4][6] Polyhydroxybutyrates are used by many bacteria for energy and carbon storage under conditions when growth is limited by elements other than carbon.[9] The authors present no mechanism by which insoluble polyhydroxybutyrate may lower the effective concentration of water in the cytoplasm sufficiently to stabilise arsenate esters. Although all halophiles must reduce the water activity of their cytoplasm by some means to avoid desiccation [10], 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. Some astrobiologists speculate that this could suggest that life can form in the absence of large amounts of available phosphorus, thus increasing the probability of finding life elsewhere in the universe.[3][4] The finding gives weight to the long-standing idea that life on other planets may have a chemical makeup differing from that of known organisms in fundamental ways, and may help in the search for extraterrestrial life.[2][3][11] 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.[12][13]

Skepticism

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][4]

In an online editorial 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."[14] University of British Columbia microbiologist Rosie 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.[15] Harvard microbiologist Alex Bradley says that arsenic-containing macromolecules such as the ones suggested in the paper would be unstable in water.[14]

See also

References

  1. ^ Davies, Paul (4 December 2010). "The 'Give Me a Job' Microbe". Wall Street Journal. Retrieved 2010-12-05.
  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 d 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. ^ a b c d e f g Bortman, Henry (2 December 2010). "Thriving on arsenic". Astrobiology Magazine. Retrieved 2010-12-04.
  5. ^ Bortman, Henry (5 October 2009). "Searching for Alien Life, on Earth". Astrobiology Magazine (NASA). Retrieved 2010-12-02.
  6. ^ a b c d e f g h i Wolfe-Simon, Felisa (2 December 2010). "A bacterium that can grow by using arsenic instead of phosphorus". Science. doi:10.1126/science.1197258. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  7. ^ 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. Retrieved 2010-12-02. {{cite journal}}: Explicit use of et al. in: |author= (help)
  8. ^ 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. Retrieved 2010-12-03.
  9. ^ 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. Retrieved 2010-12-05. {{cite journal}}: Unknown parameter |coauthors= ignored (|author= suggested) (help)
  10. ^ 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. Retrieved 2010-12-05.
  11. ^ Harvey, Mike (4 March 2010). "Could the Mono Lake arsenic prove there is a shadow biosphere?". The Times. Retrieved 2010-12-02.
  12. ^ 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.
  13. ^ 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. Retrieved 2010-12-02.
  14. ^ a b Zimmer, Carl (7 December 2010). "Scientists see fatal flaws in the NASA study of arsenic-based life". Slate. Retrieved 2010-12-07.
  15. ^ Redfield, Rosie (4 December 2010). "Arsenic-associated bacteria (NASA's claims)". RR Research blog. Retrieved 2010-12-04. {{cite web}}: External link in |work= (help)
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