A strong critique of the “arsenic paper”

I’ve rarely seen a critique this strong in the reviewed scientific literature.  It’s about Wolfe-Simon et al.’s paper in Science suggesting that a bacterium could incorporate arsenic instead of phosphorus in DNA and biomolecules.  Simon Silver and and Le T. Phung take strong issue with this in a piece in the “current controversies” section of FEMS Microbiology Letters, “Novel expansion of living chemistry or just a serious mistake?”  Simon and Phung suggest that although arsenic could have been taken up by the bacteria when they were grown in vitro, there is no evidence that it was sequestered in DNA or other places save perhaps in vesicles, where the desperate bacterium was trying to remove it.

Note, this is not post-publication peer review on a blog, but a critique in the published literature.  And it’s strong from the outset. Take a look at this abstract:

The recent online report in Science (Wolfe-Simon et al., 2010; http://www.sciencexpress.org) that a newly isolated bacterial strain can apparently replace phosphate with arsenate in cellular constituents such as DNA and RNA either (1) wonderfully expands our imaginations as to how living cells might function (as the authors and the sponsoring government agency, the USA NASA, claim) or (2) is just the newest example of how scientist-authors can walk off the plank in their imaginations when interpreting their results, how peer reviewers (if there were any) simply missed their responsibilities and how a press release from the publisher of Science can result in irresponsible publicity in the New York Times and on television. We suggest the latter alternative is the case, and that this report should have been stopped at each of several stages.

Some of the meat:

The questionable conclusion of the paper appears as an established fact in the abstract (first paragraph of the report): ‘arsenate in macromolecules that normally contain phosphate, most notably nucleic acids and proteins.’ There are no data to support this claim, which is repeated. . . . There is no reason to conclude (as the authors have in their penultimate sentence) that they have found life ‘substituting As for P’.

And the conclusion, which tries to exculpate two authors from participating in the paper’s hype (and, I believe, lay the blame for that hype at the door of Wolfe-Simon):

One caveat: we consider two of the senior-scientist authors, R.S. Oremland and J.F. Stolz, to be microbiologists who have contributed in major ways to the understanding of the environmental microbiology of arsenic in recent years (including three reports published in Science in the last 10 years and several in FEMS journals). These caused no antihype flak. We hope our long-term relationships can survive this entirely negative and uncompromising analysis of their new report, which would have been much better handled before publication (Obama style over a bottle of beer), rather than with the excessive Internet hype that the authors initiated and the controversy that developed on newspaper and journal pages. However, this is only a current example of a report, where basically no one who can form a detailed technical opinion believes the conclusions (except the authors), based on the data shown. It is a sad story, reminiscent of the quip: déjà vu – all over again!

Ouch!

___________

Silver, S. and L. T. Phung. 2011. Novel expansion of living chemistry or just a serious mistake? FEMS Microbiol. Lett 315:79-80.

23 Comments

  1. Sven DiMilo
    Posted June 7, 2011 at 5:55 am | Permalink

    Simon and and Le T. Phung take strong issue with this

    Simon Silver’s surname’s sadly skipped.

  2. daveau
    Posted June 7, 2011 at 7:41 am | Permalink

    “Ouch!” is right. But it needed to be done.

    • Posted June 7, 2011 at 8:38 am | Permalink

      Word for word, that’s almost exactly what I would have written.

      b&

  3. Hansen
    Posted June 7, 2011 at 8:31 am | Permalink

    “Obama style over a bottle of beer”

    What is that supposed to mean?

    • Posted June 7, 2011 at 8:40 am | Permalink

      For quite some time, politicians have liked to portray a folksy air whereby they suggest that the best way to settle intractable differences is to sit down with some beers and have a friendly heart-to-heart. It’s bullshit, of course, but it helps them get votes.

      Cheers,

      b&

      • Posted June 7, 2011 at 8:50 am | Permalink

        It’s much more specific than that. When a Cambridge, Mass., police officer arrested a black Harvard professor on the professor’s front porch (in the apparent belief that the house was not his), Obama sought to defuse the ensuing outcry of racism against the police and favoritism for Harvard professors by having both parties to the White House, where they discussed their differences over a couple of beers on the lawn.

        • Posted June 7, 2011 at 9:35 am | Permalink

          You’re right — I had completely forgotten about that incident. Thanks.

          b&

        • Sajanas
          Posted June 7, 2011 at 9:36 am | Permalink

          For that problem, it wasn’t a terrible solution, since it let the two take a step back and realize the fundamental humanity of their opponent.

          But this is a situation about credibility, not humanity. When researchers put their entire credibility on the line for a conclusion that they didn’t prove, and could have proved with some simple extra experiments, they crossed a personal Rubicon. They’re pretty much screwed… they can’t back down, and they can’t do much more work, since its likely they were just grasping anyway. At best they can just defend until people lose interest, and no one remembers it anymore, like those ‘bacteria’ in the Martian meteor.

        • AR
          Posted June 7, 2011 at 9:43 am | Permalink

          … Wow.

          I also was going to ask what that comment meant. Thanks Ben and Gregory for the explanation.

  4. AR
    Posted June 7, 2011 at 9:51 am | Permalink

    Yep. Ouch. But, as others have said, it needed to be said. I’m no scientist but I followed the debate on various forums and I’m pretty confident that that paper never should have been published.

    I find it interesting that the blame gets heaped squarely on W-S’ shoulders. Wonder if that’s altogether fair. I suspect W-S did play a bigger role in the pre-publication hype than did the senior-scientists (could be wrong but it seemed that way to me) but, hey, their names are on this, too. Surely they had something to do with the disaster they’ve assented to put their names on.

    Just out of curiosity from a non-scientist: is it customary in critical science reviews to call out one author among many in this way?

    • J.J.E.
      Posted June 7, 2011 at 10:17 am | Permalink

      So, the thing I would say about that “critique” is that it doesn’t rise to the level of credible technical criticism. However, this isn’t a bad thing, as the piece aspires to be a commentary rather than a careful dissection of the As paper. That’s all fine and good, but I wouldn’t cite that paper as a debunking. Rather, it expresses the well-earned skepticism and the first principles intuitions that should have given the reviewers pause in the first place. The colorful nature of the language, replete with popular culture references and singling out of individual authors, as well as the lack of references to support any of their claims signals its editorial tenor. Again, this isn’t a criticism of this paper, just a suggestion to consider its goal. It is prominently labeled as “CURRENT CONTROVERSIES IN MICROBIOLOGY” rather than a “research report”, “technical comment” or other such category (I’m not sure what categories FEMS uses). But given how apparently obvious the criticisms are (I’m not a microbiologist or an As chemist, so I take this on trust), it is a wonder that the original As paper got through basic peer review. And this take on the As paper communicates that well and entertainingly.

      However, all of the “missteps” aside, I don’t think anyone needs to be “blamed” for the As paper. Nothing bad actually happened, unless you consider a good old fashioned scientific smack-down to be a bad thing. To think otherwise is just so much pearl clutching. This is the way science works. It isn’t merely the editors and anonymous peer reviewer gatekeepers protecting the science reading public from an incessant tide of unscientific shit. No, on occasion when a published finding is simultaneously very high profile and fundamentally flawed, the scientific “immune system” goes into overdrive and the paper gets ripped to shreds in labs and journal clubs across the world. This happens on a regular basis (e.g. the kin selection debate) and is a much more transparent process than anonymous peer review prior to publication. Pre-publication peer review is essential, but post-publication peer-review is just as important. If I had to choose what kinds of errors got made, I’d prefer more bad papers got published that shouldn’t have been than more good papers get rejected that shouldn’t have been.

      • Diane G.
        Posted June 7, 2011 at 11:33 pm | Permalink

        Hear, hear to your last paragraph! It may seem to be ‘airing dirty laundry in public,’ but will serve–yet again–to show that science is an endeavor that corrects its errors.

  5. Torbjörn Larsson, OM
    Posted June 7, 2011 at 10:55 am | Permalink

    Apparently arsenic poisons everything; QED.

    From my viewpoint on the astrobiology of Davies, Lineweaver, Wolfe-Simon et al collaboration [“Signatures of a Shadow Biosphere”] that prompted this, the likelihood of variants to be found on Earth is hugely inflated considering existing competition.*

    Wishing it is so doesn’t make it so; instead you need extra-ordinary luck & evidence. It would have been very lucky to succeed in establishing some of the biological basis a few years after publishing such an heroic suggestion.

    Not that it is a bad question.

    Btw on WEIT, remarkably in the above collaboration, Davies is likely a deist (reading his books on cosmology) and has gotten criticism for his 2007 NYT article on WEIT.
    Lineweaver is, IIRC a weak and possibly erroneous memory, a theist, and at the very least an accommodationist: “INCREASINGLY OVERLAPPING MAGISTERIA OF SCIENCE AND
    RELIGION
    “, CHARLES H LINEWEAVER.
    I can’t but think that such inherent fuzzy-mindedness suggests why precisely the topic of abiogenesis makes them see invisible pink unicorns. :-/ Hopefully I’m wrong, since that is _me_ indulging in eager pattern search.

    ——–
    * [I haven’t read that paper yet, but it is now on top of my reading list. It is foremost the result that makes me believe this.]

    • Torbjörn Larsson, OM
      Posted June 7, 2011 at 11:12 am | Permalink

      Oh, btw: thanks for the heads up!

    • Sigmund
      Posted June 7, 2011 at 11:48 am | Permalink

      Paul Davies is definitely an accomodationist – he claims that Christianity set the basis for the scientific revolution.
      And he has won the Templeton prize.

    • Posted June 8, 2011 at 11:45 am | Permalink

      “Lineweaver is, IIRC a weak and possibly erroneous memory, a theist, and at the very least an accommodationist: “INCREASINGLY OVERLAPPING MAGISTERIA OF SCIENCE AND
      RELIGION“, CHARLES H LINEWEAVER.”

      I think you misjudge Lineweaver here. Have you read the paper you link to? It was Gould who claimed that religion and science are NOMA. Even the title of the paper challenges this, by saying that they overlap. In the paper, he counts himself a critic of Gould on this point.

      Maybe you thought “overlapping” means “saying the same thing” or “equally valid”. It seems that, in the paper, he challenges Gould’s claim that they are non-overlapping, which means that science can say something about fields previously the domain of religion, i.e. he seems to be on par with, say, Jerry Coyne here. I don’t see any accomodationism.

      I can see the cause of the confusion. One reaction to accomodationism is to say that there is no overlap and hence no conflict and nothing which needs to be accomodated, e.g. Gould’s NOMA. However, that doesn’t mean that if one sees an overlap, one is an accomodationist. Perhaps one says “yes, they overlap; let’s see who has the best answers”.

  6. Onkel Bob
    Posted June 7, 2011 at 11:12 am | Permalink

    I disagree that it fails to meet “credible technical criticism.” The authors make a substantial argument when they say:

    That this high arsenic may be sequestered in intracellular vesicles of unknown composition (possible) or in the cytoplasm (less likely) has not been tested. Have the authors considered that As was incorporated into phospholipids (arsenolipids) thus freeing phosphate to be used in DNA? That would lead to fragility (observed) and swelling (observed as an increase in OD). Also note the low abundance of 16S rRNA (nothing visible) and 23S rRNA genes (Fig. 2a) indicating immediate RNA turnover, possibly to facilitate reuse of limited phosphate.

    As for a “bad thing,” Science is a prestigious journal, one which rejects many of the submissions it receives. Here is an example of poor research, and even worse science, given prime real estate. Another paper, one likely with solid research and significant findings, was rejected to make room for this dreck. While this does not rise to the truly awful cases of plagiarism or data falsification, such unfounded and outlandish findings do not deserve the oxygen and attention they received.

    • J.J.E.
      Posted June 7, 2011 at 1:01 pm | Permalink

      Oh, I’m not saying that the As paper isn’t subject to credible technical criticism. But unsourced claims (there is only one reference in the piece — a reference to the FWS paper) is either commentary or bad scholarship. In this case, it is commentary, and that’s appropriate. But to make a technical criticism, one needs to rise above commentary and back up their criticisms with well-established principles in the literature. Notably, every technical comment references one or more additional sources to back up their criticisms.

      Don’t get me wrong. The As paper deserves this sort of detailed and critical dissection. Commentary is O.K. too, but it shouldn’t be confused with formal objections that are justified according to the conventions of modern scientific literature.

    • Diane G.
      Posted June 7, 2011 at 11:42 pm | Permalink

      Science also has a bit of circulation-envy for Nature, does it not? Could there be an ulterior motive of trying to publish the flashiest papers/attract the most attention, therefore, advertising?

  7. Grania
    Posted June 7, 2011 at 11:16 am | Permalink

    This is a nice example of how science corrects itself. Individual scientists may goof off and screw up or just genuinely make a mistake; but within a relatively short period of time those errors are identified and corrected.

    • Posted June 7, 2011 at 12:35 pm | Permalink

      Often those errors are identified and corrected quickly. More often errors linger for a long time. In my field someone published a data set on some strains, subsequently lost the strains, remade the strains, and the data set was not reproducible. Instead of retracting the paper, the lead author sent a letter to the community. Any non-recipient of said letter thinks the data is valid (no one has been able to repeat it). Worse, I work in this area and fear some outside expert will review my grants and criticize me for not considering this ‘published’ data set (it was published in a sexy journal).

      Worse than lingering is when piss poor studies derail funding priorities and waste scientists time showing the prior studies were wrong. The latter happens often in science but with a goal of moving knowledge forward not simply correcting someone else bullshit. XMRV-CSFis a god example of this.

  8. Sigmund
    Posted June 7, 2011 at 12:37 pm | Permalink

    I thought it was a good write up for the most part until the end.
    Why on earth did the authors feel the need to ass-kiss two of the authors of this paper? It doesn’t matter what work they did in the past, the question at hand is whether the Science paper – of which those two co-authors signed up to agreeing with – had the evidence to support its claims. If it did not then ALL the authors bear responsibility. They have the option to remove their names prior to publication.
    That said I think the real failing here is that of the peer review process in Science.
    It just goes to show that having a few big names on your paper goes a long way towards getting an easy passage though what should be a strict and potentially tortuous review process.
    If all papers got a similarly low level of scrutiny to this one we would be seeing debacles like this every week, never mind every decade.

  9. Posted June 9, 2011 at 4:23 pm | Permalink

    Okay, so it basically raises the possibility that evolution is of bacterial infection?
    It’s a good probabillty. In nature very few animals care for the young that are different and/or abnormal in any way. So bacteria or other forms of organism would gradually start an evolution on a micro scale on a long enough timeline.


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