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Deinococcus radiodurans – everyone’s favourite Archean Crazy Bacteria

Posted by Coturnix on March 21, 2007
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Researchers Uncover Protection Mechanism Of Radiation-resistant Bacterium:

Results of a recent study titled “Protein Oxidation Implicated as the Primary Determinant of Bacterial Radioresistance,” will be published in the March 20 edition of PLoS Biology. The study, headed by Michael J. Daly, Ph.D., associate professor at the Uniformed Services University of the Health Sciences (USU), Department of Pathology, shows that the ability of the bacterium Deinococcus radiodurans to endure and survive enormous levels of ionizing radiation (X-rays and gamma-rays) relies on a powerful mechanism that protects proteins from oxidative damage during irradiation.

I thought it was pretty well established that the original adaptation was against drying out (where on Earth do you get so much radiation except in the nuclear facilities built by humans over the past few decades?). The multi-level DNA repair mechanism evolved to protect DNA from dessication would work quite nicely if DNA is danaged by other causes. So, is this new study right, or the old view?

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  1. #1 greensmile
    March 21, 2007

    There is a line of speculation that the microbes you can find living on damn near nothing hundreds of feet below the surface in rock insterstices are not recently arrived inhabitants of that seemingly exotic habitat.

    There are also naturally occuring, though quite rare and not conclusively accepted, “nuclear reactors” Those I have read of were in isolated super-rich uranium ore veins in Africa. Ground water carried away the heat for centuries, as the fuel spent itself, leaving otherwise unexplainable voids and concentrations of barely soluable minerals. In THAT environment, perhaps, your question could have an answer.

  2. #2 Jonathan Eisen
    March 21, 2007

    I think it is pretty conclusive that the adaptation in the Deinococcus group is related to desiccation resistance. This is based on (1) the fact that the best place to find radiation these bugs is really dry places like the Antarctic Central valley (2) John Battista’s and others experiements showing radiation sensitive strains were also desiccation sensitive and vice versa and (3) the fact that desiccation is a common environmental phenomenon whereas expusre to radiation is not

    This study really says nothing about the desiccation theory, as the oxidative damage they are talking about occurs with radiation and desiccation. What this paper claims is that radiation resistance in various organisms is more likley due to the ability to protect and repair proteins than the ability to protect and repair DNA. It would also follow that this owuld explain desiccation resisance in many species. It does not have anything to do with WHY these organisms became resistant. It is just about the mechanism. I am not convinced about the mechanism, by the way. But even if they are right, it does not say anything about what drove these organisms to become resistant

  3. #3 coturnix
    March 21, 2007

    Thank you – this is exactly the kind of explanation I was looking for.

  4. #4 Bill
    March 21, 2007

    What this paper claims is that radiation resistance in various organisms is more likley due to the ability to protect and repair proteins than the ability to protect and repair DNA.

    That’s how I read it also. I’m not convinced either. What profiteth it a microorganism, specifically the generation *after* exposure, if it protect its proteins and lose its genomic integrity? Further, a cell typically has a great many copies of any given protein on hand, but only one copy of its genome.

  5. #5 coturnix
    March 21, 2007

    Yup, more I think about this, more fishy it appears.

  6. #6 Mike Daly
    March 21, 2007

    These are early days in the investigation. What I can say is that we have looked at the level of oxidative protein damage caused by desiccation in resistant and sensitive bacteria, and a simililar relationship holds. This work is being prepared for publication. I agree with Jonathan that the evolution of extreme ionizing radiation resistance had little, if anything to do with ionizing radiation. We have not yet looked at levels of oxidative protein damage in response to UV. By the way, Deinococcus belongs to the Kingdom: Bacteria.

  7. #7 coturnix
    March 21, 2007

    Really? It is not an Archaean?

    Perhaps proteins need to be resistant so they can efficiently do the DNA repair?

  8. #8 Mike Daly
    March 21, 2007

    Here are 2 links to well-written summaries of the work, including comments by Battista in the online Science review:

    http://biology.plosjournals.org/perlserv/?request=get-document&doi=10.1371/journal.pbio.0050108

    http://sciencenow.sciencemag.org/cgi/content/full/2007/320/2

  9. #9 Jonathan Eisen
    March 21, 2007

    By the way – it is so cool that the author of the paper posted here …

    Michael – very very happy to see that you published this in PLoS Bio. And even though I am not convinced as of now, very interesting idea. I will have to read more carefully and ponder more before saying for real whether I am convinced or not.

  10. #10 coturnix
    March 21, 2007

    I know – it is so cool. And it is happening more and more often these days. Paper publication always leaves something out, a part of the story that goes unreported – so it is always great to see the author come and bring in the missing pieces of the puzzle.

  11. #11 Mike Daly
    March 21, 2007

    To the host of this blog, I spent 4 years in Beograd as a child and later 4 years in Zagreb. Very fond memories.

  12. #12 greensmile
    March 21, 2007

    IANAB but it costs nothing to ask:)

    If some source of radiation were [definitely time to use the subjunctive] an environmental factor that spurred the evolution of the resistance, then several other factors would have to be accounted for and I have no idea of what the data are:
    1. when did the resistance show up in the history [which is related closely to and might only be infered from]
    2. what is the pattern of heiritance and spread [I already used up "radiation"] of the trait. Any sign of convergence?
    3. intermittent drought…which is a micro envrionment that has been scattered around the planet and throughout the eras would be how much more common than local radiation sources?

    The idea that radiation could have driven this, I am agreeing, fails occams razor and will probably fail other specific tests.
    What chemistry can go on when a bacteria is in a desiccated state? [other than oxidation...which probably goes on in the wet and living citter very effectively as well] Is the repair mechanism only active as the organism is rehydrated or is it some kind of xerochemistry that I can’t imagine…[or when you all say "dessication" you mean "relatively" dry, not absolutely dry as the word implies to the casual reader?]

    As quickly as bacteria develop antibiotic resistance, I would expect that simply planting a few hundred petri dishes around a canister of radium and letting things ferment, you’d either show that it is not easy to develop radiation resistance by using radiation as a selection pressure [fitting the theory I see here] or it does develop [giving you a problem that further experiments would have to pick apart.]

  13. #13 Mike Daly
    March 21, 2007

    Some quick answers in response to Greensmile’s questions:

    Horizontal gene transfer makes it difficult to put an age on Deinococcus.

    Re: convergence. Jonathan may know. It is still not established that DNA repair systems alone are responsible for resistance. And, there is always the possibility that different radiation/desiccation resistant bacteria have evolved very differently. But I don’t think so.

    As cells desiccate (dry), they begin to ‘deflate’ and many reactive surfaces and proteins within the cells are squashed together generating oxidative stress (reactive oxygen radicals).

    In 1961, Erdman et al reported the directed evolution of radiotolerance in E. coli by the repeated passage of resistant survivors through successive sublethal doses of 60Co irradiation. This work was followed in 1974 by similar studies and results published by Parisi and Antoine on Bacillus pumilus. The increase in resistance of B. pumilus was accompanied by a corresponding increase in spore resistance through the seventh irradiation passage. By the fifteenth passage, the ability for spore formation was lost, but the resistance of vegetative cells was further increased. Notably, B. pumilus cells with increased ionizing radiation (IR) resistance became auxotrophic for (no longer could make) sulfurous and branched-chain amino acids, and nicotinic acid-related vitamins. Sort of like D. radiodurans naturally is. Reducing the amount of metabolic work those cells have to do after irradiation would lower the production of free radicals generated by metabolism, which would better position the cells to survive radiation-induced radicals. The stepwise approach to selecting bacterial radioresistance was validated once more in 2005 by Battista, where the radioresistance of an IR-selected E. coli strain was ~500-fold more resistant at 5,000 Gy than its parent. But this still did not even approach the resistance of D. radiodurans. We have done similar experiments, but after a certain number of rounds of IR selection no further increases in resistance were observed. So, radiation resistance is more than simply selecting the ‘right’ metabolic configuration, and certainly not like antibiotic resistance.

    Ignoring IR for the moment, when did resistance to reactive oxygen species (ROS) first occur? Probably early in the history of Earth. Unlike today, the early oceans were full of dissolved iron, which gives rise to the same sort of ROS that ionizing radiation generates. Ancient cells were probably very iron-rich. Even though O2 was absent, hydrogen peroxide would have been generated by UV in cells at the ocean’s surface. H2O2 + Fe generates ROS, but Mn can eliminate a subset of those ROS which damage proteins. In ancient cells, Mn cycling might have filled in for enzyme-based ROS scavenging systems which evolved later. Give the amount of dissolved iron around billions of years ago, I expect that DNA repair systems worked very efficiently even then. As enzyme systems that protect proteins from oxidative damage evolved, and most of the dissolved iron disappeared from the oceans, Mn-redox-based protection systems disappeared, except for cells which had moved to the land and were exposed to a new source of ROS during desiccation. It’s possible that those ancient DNA repair systems retain the potential to work very efficiently in modern cells provided they are allowed to work in the right environment. This argument is strengthened by the fact that several DNA repair genes from radiation sensitive bacteria can functionally replace DNA repair genes in Deinococcus.