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DBL%20Hendrix%20small.png College chemistry, 1983

Derek Lowe The 2002 Model

Dbl%20new%20portrait%20B%26W.png After 10 years of blogging. . .

Derek Lowe, an Arkansan by birth, got his BA from Hendrix College and his PhD in organic chemistry from Duke before spending time in Germany on a Humboldt Fellowship on his post-doc. He's worked for several major pharmaceutical companies since 1989 on drug discovery projects against schizophrenia, Alzheimer's, diabetes, osteoporosis and other diseases. To contact Derek email him directly: derekb.lowe@gmail.com Twitter: Dereklowe

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December 7, 2010

Arsenic Bacteria: Does The Evidence Hold Up?

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Posted by Derek

It's time to revisit the arsenic-using bacteria paper. I wrote about it on the day it came out, mainly to try to correct a lot of the poorly done reporting in the general press. These bacteria weren't another form of life, they weren't from another planet, they weren't (as found) living on arsenic (and they weren't "eating" it), and so on.

Now it's time to dig into the technical details, because it looks like the arguing over this work is coming down to analytical chemistry. Not everyone is buying the conclusion that these bacteria have incorporated arsenate into their biomolecules, with the most focused objections being found here, from Rosie Redfield at UBC.

So, what's the problem? Let's look at the actual claims of the paper and see how strong the evidence is for each of them:

Claim 1: the bacteria (GFAJ-1) grow on an arsenate-containing medium with no added phosphate. The authors say that after several transfers into higher-arsentic media, they're maintaining the bacteria in the presence of 40 mM arsenate, 10 mM glucose, and no added phosphate. But that last phrase is not quite correct, since they also say that there's about 3 micromolar phosphate present from impurities in the other salts.

So is that enough? Well, the main evidence is that (as shown in their figure 1), that if you move the bacteria to a medium that doesn't have the added arsenate (but still has the background level of phosphate) that they don't grow. With added arsenate they do, but slowly. And with added phosphate, as mentioned before, they grow more robustly. It looks to me as if the biggest variable here might be the amount of phosphate that could be contaminating the arsenate source that they use. But their table S1 shows that the low level of phosphate in the media is the same both ways, whether they've added arsenate or not. Unless something's gone wrong with that measurement, that's not the answer.

One way or another, the fact that these bacteria seem to use arsenate to grow seems hard to escape. And they're not the kind of weirdo chemotroph to be able to run off arsenate/arsenite redox chemistry (if indeed there are any bacteria that use that system at all). (The paper does get one look at arsenic oxidation states in the near-edge X-ray data, and they don't see anything that corresponds to the plus-3 species). That would appear to leave the idea that they're using arsenate per se as an ingredient in their biochemistry - otherwise, why would they start to grow in its presence? (The Redfield link above takes up this question, wondering if the bacteria are scavenging phosphorus from dead neighbor cells, and points out that the cells may actually still be growing slowly without either added arsenic or phosphate).

Claim 2: the bacteria take up arsenate from the growth medium. To check this, the authors measured intracellular arsenic by ICP mass spec. This was done several ways, and I'll look at the total dry weight values first.

Those arsenic levels were rather variable, but always run high. Looking at the supplementary data, there are some large differences between two batches of bacteria, one from June and one from July. And there's also some variability in the assay itself: the June cells show between 0.114 and 0.624% arsenic (as the assay is repeated), while the July cells show much lower (and tighter) values, between 0.009% and 0.011%. Meanwhile, the corresponding amount of phosphorus is 0.023% to 0.036% in June (As/P of 5 up to 27), and 0.011 to 0.014 in July (As/P of 0.76 to 0.97).

The paper averages these two batches of cells, but it certainly looks like the June bunch were much more robust in their uptake of arsenate. You might look at the July set and think, man, those didn't work out at all, since they actually have more phosphorus than arsenic in them. But the background state should be way lower than that. When you look at the corresponding no-arsenic cell batches, the differences are dramatic in both June and July. The June batch showed at least ten times as much phosphorus in them, and a thousand times less arsenic, and the July run of no-arsenate cells showed (compared to the July arsenic bunch) 60 times as much phosphorus and 1/10th the arsenic. The As/P ratio for both sets hovers around 0.001 to 0.002.

I'll still bet the authors were very disappointed that the July batch didn't come back as dramatic as the June ones. (And I have to give them some credit for including both batches in the paper, and not trying just to make it through with the June-bugs). One big question is what happens when you run the forced-arsenate-growth experiment more times: are the June cells typical, or some sort of weird anomaly? And do they still have both groups growing even now?

One of the points the authors make is that the arsenate-grown cells don't have enough phosphorus to survive. Rosie Redfield doesn't buy this one, and I'll defer to her expertise as a microbiologist. I'd like to hear some more views on this, because it's a potentially important. There are several possibilities - from most exciting to least:

1. The bacteria prefer phosphorus, but are able to take up and incorporate substantial amounts of arsenate, to the point that they can live even below the level of phosphorus needed to normally keep them alive. They probably still need a certain core amount of phosphate, though. This is the position of the paper's authors.

2. The bacteria prefer phosphorus, but are able to take up and incorporate substantial amounts of arsenate. But they still have an amount of phosphate present that would keep them going, so the arsenate must be in "non-critical" biochemical spots - basically, the ones that can stand having it. (This sounds believable, but we still have to explain the growth in the presence of arsenate).

3. The bacteria prefer phosphorus, but are able to take up and incorporate substantial amounts of arsenate. This arsenate, though, is sequestered somehow and is not substituting for phosphate in the organisms' biochemistry. (In this case, you'd wonder why the bacteria are taking up arsenate at all, if they're just having to ditch it. Perhaps they can't pump it out efficiently enough?) And again, we'd have to explain the growth in the presence of arsenate - for a situation like this, you'd think that it would hurt, rather than help, by imposing an extra metabolic burden. I'm assuming here, for the sake of argument, that the whole grows-in-the-presence-of-arsenate story is correct.

Claim 3: the bacteria incorporate arsenate into their DNA as a replacement for phosphate. This is an attempt to distinguish between the possibilities just listed. I think that authors chose the bacterial DNA because DNA has plenty of phosphate, is present in large quantities and can be isolated by known procedures (as opposed to lots of squirrely little phosphorylated small molecules), and would be a dramatic example of arsenate incorporation. These experiments were done by giving the bacteria radiolabeled arsenate, and looking for its distribution.

Rosie Redfield has a number of criticisms of the way the authors isolated the DNA in these experiments, and again, since I'm not a microbiologist, I'll stand back and let that argument take place without getting involved. It's worth noting, though, that most (80%) of the label was in the phenol fraction of the initial extraction, which should have proteins and smaller-molecular-weight stuff in it. Very little showed up in the chloroform fraction (where the lipids would be), and most of the rest (11%) was in the final aqueous layer, where the nucleic acids should accumulate. Of course, if (water-soluble) arsenate was just hanging around, and not being incorporated into biomolecules, the distribution of the label might be pretty similar.

I think a very interesting experiment would be to take non-arsenate-grown GFAJ-1 bacteria, make pellets out of them as was done in this procedure, and then add straight radioactive arsenate to that mixture, in roughly the amounts seen in the arsenate-grown bacteria. How does the label distribute then, as the extractions go on?

Here we come to one of my biggest problems with the paper, after a close reading. When you look at the Supplementary Material, Table S1, you see that the phenol extract (where most of the label was), hardly shows any difference in total arsenic amounts, no matter if the cells were grown high arsenate/no phosphorus or high phosphorus/no arsenate. The first group is just barely higher than the second, and probably within error bars, anyway.

That makes me wonder what's going on - if these cells are taking up arsenate (and especially if they grow on it), why don't we see more of it in the phenol fraction, compared to bacteria that aren't exposed to it at all? Recall that when arsenic was measured by dry weight, there was a real difference. Somewhere there has to be a fraction that shows a shift, and if it's not in the place where 80% of the radiolabel goes, then were could that be?

I think that the authors would like to say "It's in the DNA", but I don't see that data as supporting enough of a change in the arsenic levels. In fact, although they do show some arsenate in purified DNA, the initial DNA/RNA extract from the two groups (high As/no P and no As/high P) shows more arsenic in the bacteria that weren't getting arsenic at all. (These are the top two lines in Table S1 continued, top of page 11 in the Supplementary Information). The arsenate-in-the-DNA conclusion of this paper is, to my mind, absolutely the weakest part of the whole thing.

Conclusion: All in all, I'm very interested in these experiments, but I'm now only partly convinced. So what do the authors need to shore things up? As a chemist, I'm going to ask for more chemical evidence. I'd like to see some mass spec work done on cellular extracts, comparing the high-arsenic and no-arsenic groups. Can we see evidence of arsenate-for-phosphate in the molecular weights? If DNA was good enough to purify with arsenate still on it, how about the proteome? There are a number of ways to look that over by mass-spec techniques, and this really needs to be done.

Can any of the putative arsenate-containing species can be purified by LC? LC/mass spec data would be very strong evidence indeed. I'd recommend that the authors look into this as soon as possible, since this could address biomolecules of all sizes. I would assume that X-ray crystallography data on any of these would be a long shot, but if the LC purification works, it might be possible to get enough to try. It would certainly shut everyone up!

Update: this seems like the backlash day. Nature News has a piece up, which partially quotes from this article Carl Zimmer over at Slate.

Comments (35) + TrackBacks (0) | Category: Biological News | General Scientific News


COMMENTS

1. RB Woodweird on December 7, 2010 12:00 PM writes...

How about using radioactive arsenic?

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2. RB Woodweird on December 7, 2010 12:04 PM writes...

Sorry. That was suggested in the blog. I did not read for comprehension.

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3. road on December 7, 2010 12:06 PM writes...

The question is: should the reviewers have let the paper in, in it's current form?

I for one don't see how they could've let it in without requiring a few more controls -- especially basic LC-MS of some biomolecules. It's not like those are difficult/exotic experiments, when compared to the ones they included in the paper.

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4. Carl Zimmer on December 7, 2010 12:06 PM writes...

I talked to a bunch of microbiologists for a new piece just up on Slate: slate.com/id/2276919/ They're pretty down on the paper, to say the least.

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5. Curryworks on December 7, 2010 12:08 PM writes...

If this paper gets debunked then they can try to use the As in a Pb free cross-coupling and publish the results in JACS (only to have it further retracted b/c of trace Pb levels). The idea of impurities is lost on most people

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6. yonemoto on December 7, 2010 12:21 PM writes...

Mass spec and HPLC are really difficult techniques to prove this. The easiest, and I have said this many times, is density gradient ultracentrifugation. It's an old, very "pure bio" technique, and it's easy (if forgotten).

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7. Jim Hu on December 7, 2010 12:28 PM writes...

MS should work on oligos derived from the DNA. If the DNA is resistant to enzymatic and chemical cleavage, that might support the authors. If not, separate and fly the products.

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8. MoMo on December 7, 2010 12:34 PM writes...

This whole idea that As can substitute for P is specious at best and leads our great Society astray. No doubt sensationalized by overactive PR people at the University level.

Where's the ATA instead of ATP? What about ADA instead of ADP and other energy currencies? Huh? Then the energy of the diphosphate vs the diarsenate? Huh?

You can fool some of the people some of the time but very few chemists and microbiologists are buying into this dumbed down version of what the paper really said.

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9. Curious Wavefunction on December 7, 2010 1:01 PM writes...

The explanation I still think is most likely is that the bacteria get fanatically efficient at mopping up trace quantities of phosphorus. That would be consistent with the principles of evolution and with Occam's Razor.

Important processes might be getting down-regulated to the minimal level necessary for survival. For instance the number of key proteins and organelles including ribosomes might be getting reduced to a minimum necessary for supporting survival.

This would also explain your big question, which is why there seems to be the same amount of arsenate in both cases (As+/P- and As-/P+). If we assume that the arsenic does not get actively incorporated but only non-covalently sticks to biomolecules and hangs around in the periphery, then its concentrations should indeed stay similar in the two instances.

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10. MoMo on December 7, 2010 1:11 PM writes...

That's right Curious Waveform. E. coli can grow in 18 megaohm distilled water, forming biofilms with reckless abandon. Then there is the fact that you have to go through ass-pain heaven using scavenging resins to sequester all the random gegen-ions in media used in anabolism experiments. Did they do this? NO!

More bad science! But what do you expect from the government?
Move On Derek!

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11. Curt F. on December 7, 2010 1:20 PM writes...

Derek, a great post today. One question on an issue of lesser importance: where did you learn of the critique at http://rrresearch.blogspot.com/2010/12/arsenic-associated-bacteria-nasas.html? Was it from commenter Paul writing at your own blog (http://pipeline.corante.com/archives/2010/12/02/life_with_arsenic_whod_have_thought.php#464464)? What about the possibility of LC-MS? Did you learn of it from commenter noname or from anyone else in that prior thread?

I know it's your blog and you can do what you want...but if your post today was inspired, in part, by these and other comments, it would be nice to see an acknowledgement of that fact. Several people (myself included) put some serious thought into their comments, and several others took the time to contribute really useful links to external critiques.

If, on the other hand, you weren't inspired by the other thread, why not? Do you usually read the comments? Are we wasting our time if we try to try to type out anything besides jokes and snark?

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12. Jordan on December 7, 2010 1:23 PM writes...

There's also the issue (brought up by another blogger -- was it Chembark?) that arsenate esters aren't very stable to begin with, and hydrolyze much faster than phosphate esters. Makes one wonder whether arsenate-based DNA could even be detected in a gel to begin with.

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13. JamesM on December 7, 2010 1:41 PM writes...

Alex Bradley posted some further objections:

http://scienceblogs.com/webeasties/2010/12/guest_post_arsenate-based_dna.php

A summary of his points:

1. once any As-based DNA was in water as part of the phenol-chloroform extraction, bereft of any protective cellular machinery, it should have hydrolysed to very small fragments, not the 10,000 nucleotide fragment their Figure 1 shows.

2. Therefore the As detected by the elemental analysis is that hanging around non-specifically in the agarose gel, not part of a DNA backbone.

3. Bacteria in the Sargasso Sea cope with even lower levels of phosphate than 3uM, by removing P from their lipids -- but not DNA.

Worth a read.

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14. Anonymous on December 7, 2010 2:13 PM writes...

The last author on the Science paper (Ron Oremland) just gave a talk on NASA-TV about this work. You might be able to still watch it online. The performance was not encouraging for those who want to believe this is real.

He spent maybe 15 minutes talking about the actual data in the paper and offered no real defense against the criticisms. The talk itself was very weird -- non-stop folksy jokes and irrelevant digressions, with only minimal substance (examples of digression: meandering discussion of Chairman Mao; arguing that people should not criticize the paper because his postdoc is much cheaper than space exploration).

You get the sense that he is in way over his head, just completely lost.

The Q&A starts right now.

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15. Anonymous on December 7, 2010 2:28 PM writes...

examples of Oremland's responses to questions from the talk (some paraphrased as best as I can; watch it for yourself on the NASA website).

1) "Where is my brisket?" (Oremland had been joking about pastrami sandwiches throughout the talk; the questioner was asking about DNA, not food).

2) "We don't know. That would take decades of work." (In response to a question about what was contained in the vacuoles of his arsenic fed bacteria.)

3) "These aren't even back of the envelope calculations. They are inside the envelope calculations." (in response to complaints that the published estimates of arsenic in the DNA are not accurate)

4) "This is really about the number of angels that you can fit on the head of a pin...do you want white bread or pastrami for your sandwich?" (in response to another question about arsenic in DNA, not food).

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16. Pharmaheretic on December 7, 2010 2:47 PM writes...

It seems that most so-called 'scientists' are ignoring something very basic here.

That organism can survive at levels of intracellular arsenic (and low phosphorous) which were hitherto considered to be outside the realm of possibility. The very fact that conventional earth-based life can adapt to survive under such extreme chemical conditions is a sign that a far wider range of biochemistry is viable.

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17. RB Woodweird on December 7, 2010 3:21 PM writes...

They actually did use radioactivity. From Professor Redfield's blog, linked to above:

"The authors then grew some cells with radioactive arsenate (73-As) and no phosphate, washed and dissolved them, and used extraction with phenol and phenol:chloroform to separate the major macromolecules. The protein fraction at the interface between the organic and aqueous phases had about 10% of the arsenic label but, because the interface material is typically contaminated with liquid from the aqueous phase, this is not good evidence that the cells' protein contained covalently-bound arsenate in place of phosphorus. About 75% of the arsenic label was in the aqueous (upper) fraction. The authors describe this fraction as DNA/RNA, but it also contains most of the small water-soluble molecules of the cell, so its high arsenic content is not evidence that the DNA and RNA contain arsenic in place of phosphorus. The authors use very indirect evidence to argue that the distribution of arsenic mirrors that expected for phosphate, but this argument depends on so many assumptions that it should be ignored."

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18. qetzal on December 7, 2010 4:02 PM writes...

Dr. Redfield offers another, better argument against As in the DNA. The authors gel purified DNA from bugs grown either -As/+P, or +As/-P. Then they used MS to determine As:C ratios in each purified DNA fraction. For bugs grown +As/-P, the ratio was 13.4 x 10^-6. That was only twice the ratio seen with bugs grown -As/+P!

More importantly, The normal P:C ratio in DNA is about 0.1. Thus, even if we accept that the As is in the DNA (and not some contaminant carried over during gel purification), it's only enough to represent ~ 1 As per 5000 base pairs.

Even if there really is 1 As/5000 bp, that might simply represent the equivalent of unrepaired DNA damage. As an analogy, if we irradiated some bugs with UV, we might find that they grew really slowly, and we might find that they had ~ 1 thymine dimer per 5000 bp, simply because their DNA repair machinery was having a hard time keeping up with the level of UV damage. We wouldn't consider that as evidence that the bugs had learned to use TT dimers in their DNA.

I wonder if the same general objection might apply elsewhere? E.g., there might well be some As in the proteins & lipids, but that doesn't mean the bug is actively "using" As that way. It could just mean the bug is good at tolerating As, and at making due with minimal P.

From what I've seen so far, the only result that's hard to dismiss as artifact is that the bugs grew +As/-P, but not -As/-P.

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19. Anonymous on December 7, 2010 4:18 PM writes...

The suggestion was made in comments in Redfield's blog that there may really be no difference in cell proliferation in +As/-P versus -As/-P media. The authors determined those growth curves by measuring OD660 and acridine orange staining. Neither of those is really a direct measure of viable cell number (compared to for example cfu). Both could give the false appearance of cell growth because the bacteria take up lots of arsenic in the +As/-P condition, this results in a large increase in cell size as the authors showed, and this increase in size would increase the OD660 absorbance and could also make the cells stain more strongly for acridine, which would affect the cell counts. Shouldn't happen if you are careful, but...

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20. Mike on December 7, 2010 4:59 PM writes...

Pharmaheretic,
It is not accurate to say that bacteria which can survive arsenic "were hitherto considered to be outside the realm of possibility". Bacteria of the genus Halomonas, which can tolerate high concentrations of arsenic, have been known and studied for decades.

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21. SteveM on December 7, 2010 6:30 PM writes...

Maybe the investigators are in training for Big Pharma ghost writing jobs...

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22. leftscienceawhileago on December 7, 2010 8:34 PM writes...

Hmm,
I think a doable experiment (that would be reasonably sensitive to partial incorporation) would be fiber diffraction on the plasmid.

The presence of arsenic would correspond to anomalous differences for the meridional reflections.

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23. chode on December 7, 2010 11:53 PM writes...

umm, what about the synchrotron x-ray evidence in the paper that everyone conveniently overlooks because they don't understand. Pretty convincing evidence of the authors' claims.

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24. Rock on December 8, 2010 12:39 AM writes...

Their big mistake was not using alkalinized water which would have aided in the absorption of the arsenic.

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25. Paul on December 8, 2010 12:54 AM writes...

Chode: Redfield doesn't ignore it:

"Finally, the authors examined the chemical environment (neighbouring atoms and bonds) of the arsenic in the cells using synchrotron X-ray studies. This is over my head, but they seem to be trying to interpret the signal as indicating that the environment of the arsenic is similar to that of phosphorus in normal DNA. But the cellular arsenic being in DNA can't be the explanation, because their DNA analysis indicated that very little of the cellular arsenic purifies with the DNA. The cells contained 0.19% arsenic (1.9x10^6 ppb), but the DNA only contained 27 ppb arsenic."

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26. chode on December 8, 2010 1:16 AM writes...

@Paul thats exactly my point, Redfield doesn't understand the implications of this data and freely admits it.

Very little of the cellular As purifies with DNA but how much of total cellular P is in the DNA fraction? A likewise tiny amount, but thats beside the point. Its hard to mistake what the synchrotron data says about the structure of these molecules.

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27. Yggdrasil on December 8, 2010 1:52 AM writes...

@chode, the x-ray spectroscopy data gives bond distances consistent with those expected from DNA, but DNA is not the only molecule which would be expected to show these types of spectra. For example, I don't see how arsenylated nucleotides would give a signal distinct from that of arsenylated DNA. While this provides nice evidence for arsenic incorporation (and good evidence against arsenic acting as an energy source for the bacteria), it does not provide direct evidence of As incorporation into DNA, the most controversial claim of the paper.

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28. chode on December 8, 2010 2:20 AM writes...

so there is nice evidence for As incorporation into biomolecules, and this alone does not provide direct evidence of As in DNA but what about this evidence in conjunction with the 73As evidence and you start to see a general trend in the data toward the authors' interpretation. No its not iron clad but its certainly a plausible explanation of the data that is there for the community to prove or disprove.

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29. Reave on December 8, 2010 4:53 AM writes...

"And they're not the kind of weirdo chemotroph to be able to run off arsenate/arsenite redox chemistry (if indeed there are any bacteria that use that system at all)."

There are bacteria that utilize arsenate as a terminal electron acceptor, reducing it to arsenite, including some in the Geobacter, if memory serves. This is a major mechanism for the mobilization of arsenic in groundwater, in fact.

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30. Anonymous on December 8, 2010 9:05 AM writes...

the x-ray data is not from purified material. any claims about specific biomolecules is just speculation until they actually purify a specific biomolecule and characterize it.

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31. rhodium on December 8, 2010 10:12 AM writes...

It seems the skeptics make a very strong case. Biochemistry adapts to what works in aqueous solution, so Claisen reactions but no Grignards (although nature can sequester oxygen sensitive cofactors in anaerobic environments). Given the kinetics of arsenate hydrolysis, As-based DNA is just too reactive to exist for very long and As-based RNA is completely unbelievable. Anybody want to speculate on the half-life of an As analog RNA dinucleotide?
What I find most unfortunate is that NASA is involved in global climate monitoring. When this work is shown to be incorrect, it will encourage critics to paint all of NASA's research and data as unreliable.

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32. coprolite on December 8, 2010 12:42 PM writes...

Those are some good points, MoMo.

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33. Curt F. on December 8, 2010 1:58 PM writes...

any claims about specific biomolecules is just speculation until they actually purify a specific biomolecule and characterize it.

I don't agree with the idea that any and all possible claims about specific biomolecules are "speculation" until the molecules are purified. What if more X-ray modeling showed that only arsenylated DNA gave rise to the observed X-ray spectrum? What if they did NMR experiments on whole cells and found clear evidence of arsenylation?

Do you think that claims about the composition of say the sun is "speculation" until various components of sun are purified?

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34. jb on December 8, 2010 4:01 PM writes...

Not an expert here so I'm just reading the comments. This brings a question of how many supposedly "groundbreaking" research made it to the lay media but turned out to be duds. This is like peeing before you get to the toilet.

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35. BoredChemist on December 9, 2010 11:01 AM writes...

While the experimental fallacies in the suspect article appear to be glaring, I'm most disconcerted by the epic failure of peer review. Perhaps Science is trying to spark debate by publishing controversial results; however, I think shady research does more to damage prestige and credibility. Plus, research controversies and scandals give political extremists more excuses to cut public funding of science.

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