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Monday, May 06, 2013

Hydrogen Peroxide Powers Evolution

I'm about to offer a conjecture that is a bit preposterous-sounding but could well hold true. I actually think it does.

I propose that evolution, at the level of bacteria (though probably not at higher levels), is driven by hydrogen peroxide.

This theory rests on three assumptions: One is that the creation of new bacterial species happens almost entirely via lateral gene transfer, not heritable point-mutations. Secondly, bacteria (marine and terrestrial) are regularly exposed to challenges by hydrogen peroxide in the environment. Thirdly, those challenges drive lateral gene transfer.

Evidence for the first assumption is embarrassingly abundant. If you're not up to speed on the subject, I suggest you read the excellent paper, "Lateral Gene Transfer," by Olga Zhaxybayeva and W. Ford Doolittle in Current Biology, April 2011, 21:7, pp. R242-246 (unlocked copy here). It's now common to find that any given bacterial species can trace a good percentage of its protein base to "ancestors" that are too far removed horizontally to be ancestors in the conventional sense.

Consider E. coli. There are hundreds of strains of E. coli, with genes ranging in number from 4,100 to about 5,300 per strain. The problem is, the various strains of E. coli have only about 900 genes in common (and that's far too few genes to render a fully functional E. coli). The E. coli pan-genome actually takes in more than 15,000 gene families, total. Certainly, you can draw a family tree of E. coli based on 16S ribosomal polymorphisms, but that doesn't explain where the 15,000 pan-genome genes came from. The "family tree" metaphor quickly breaks down if you start drawing trees based on proteins. You get many conflicting trees—all of them correct.

Trees like this are fiction where bacteria are concerned.
The tree of life is more like a net of life or web
of life than a directed acyclic graph.
Where are all of the genes coming from? Other species, of course. They arrive by way of mechanisms like transformation, transduction, and conjugation. all of which allow direct entry of foreign DNA into a bacterial cell. At one time it was thought that conjugation could only occur between bacteria of the same species, but it is now known that cross-species conjugation also occurs (as, for example, between E. coli and Streptomyces or Mycobacterium).

Transduction, which is where viruses package up an infected host's genes in virus capsules that are then taken up by another cell, occurs naturally in bacterial populations in response to environmental factors like ultraviolet light and hydrogen peroxide. Exposure of a virus-carrying (lysogenic) cell to UV light or peroxide can induce runaway production of virus, and in fact this mechanism is used by Streptococcus to kill competitive Staphylococcus cells, in a clever bit of chemical warfare. It's been known for years that hydrogen peroxide can cause many types of bacteria to shed DNA. Now we know why: Hydrogen peroxide is a signalling molecule. It signals (among other things) lysogenic bacteria to go into a lytic cycle. It also signals cells to mount what's known as the SOS response, which is a global response to oxidative challenge. Years ago, Bruce Ames and his colleagues showed that exposing Salmonella to very dilute (60 micromolar) hydrogen peroxide caused the cells to differentially express 30 "SOS" proteins, including heat-shock proteins and low-fidelity DNA-repair systems. We know that hydrogen peroxide as dilute as 0.1 micromolar can induce phage (virus) production in up to 11% of marine bacteria. This is significant, because rainwater contains hydrogen peroxide in concentrations of 2 to 40 micromolar, and ocean water has been known to reach millimolar levels of H2O2 after a rain storm.

If you're wondering why rain contains hydrogen peroxide, the peroxide gets there in two ways. One is UV-frequency photochemistry (where water is cleaved to H and OH, then reforms as H2 and H2O2); the other is via ionization reactions caused by lightning. (Lightning is energetic enough to bring airborne oxygen and water to a plasma state. The resulting ionization and rearrangement of free atoms yields a certain amount of hydrogen peroxide.) The presence of H2O2 in rainwater has been confirmed many times, and in fact there's a well-preserved "fossil record" of it in polar icepacks, going back centuries. (Polar snowpacks contain from 10 to 900 ppb of H2O2; it varies seasonally, the max coming in summer.)

Bottom line, every rain event (over land, over sea) constitutes a hydrogen peroxide challenge for microbes. Which induces viral transduction (and a release of whole-cell DNA through lysis, some of which will be inevitably be used in transformation). It also induces low-fidelity DNA repair (which is guaranteed to help evolution along). Every rain event, in other words, is a chance for evolution to do its thing. For bacteria, that means gene-sharing within and across species lines.
Darwin's theory of a tree-like ancestor basis
for all living things is dead wrong, at
least for bacteria.
W. Ford Doolittle (who wrote a classic book chapter about lateral gene transfer called "If the Tree of Life Fell, Would We Recognize the Sound?") estimates that if a horizontal gene transfer occurs once every ten billion vertical replications, "it would be enough to ensure that no gene in any modern genome has an unbroken history of vertical descent back to some hypothetical last universal common ancestor." (See this article.)

It's obvious (to me, at least) that every rain event carries with it the potential to cause far more gene transfers than are necessary (according to Doolittle) to make vertical inheritance fade into insignificance as an evolutionary bringer of change. The hydrogen peroxide in rain has been driving lateral gene transfer in bacteria for eons. In fact, it is arguably the dominant driver of evolution in bacteria.

Sorry, Mr. Darwin. Point mutations handed down to sons and daughters just isn't cutting it.

1 comment:

  1. Thanks for this note :-) Some rigorous and boring scientific stuff, well digested for the lay reader... I've enjoyed reading it very much.

    I recall back in 1998-ish at school, I found a someone's thesis dealing with ANN evolution using genetic algorithms. Similar to this blog, it was not a proper incomprehensible science paper - rather, it was all pretty understandable, with a clear argument structure. I cannot find that particular thesis anymore, I have a faint recollection that it was from someone in the Netherlands or Sweden or thereabouts... perhaps one of the first papers on the topic available for free on the interwebs, found via webcrawler or what. Nowadays, using all the right keywords, Google returns a zillion references to prior and later sources on the topic, proper scientific papers in redacted magazines...

    Anyway my point is: the ANN/GA paper explained with great patience, that point mutations are not a very useful evolutionary mechanism, that it doesn't help if you increase the point mutation probability, that they should be used as precious spice, just a grain of salt - and praised, you guessed it, the "crossover operator", as the evolution workhorse: the mechanism that rehashes or cuts and pastes snippets of genetic code from two previous-generation individuals to the curent-generation individual. The author argued and demonstrated on some stats that the crossover operator (even very crude and low-level, ignoring higher-level semantics of the genetic code, or even all the better that way) was surprisingly efficient in "escaping from the traps of local optima" / generating globally better "innovative" solutions and whatnot.

    I guess he even went on to mention biological analogies (and their limits) - saying that two complementary genders (although being favoured by evolution in nature) are not in any way required for the crossover mechanism to work in ANN/GA models, but that the natural crossover capability is a boon for biological organism species that do evolve in bipolar genders = that need two ancestors to produce offspring.

    I don't recall the author explicitly stating something like "poor unicellular organisms, they're limited to random mutations" - but that was effectively one of the partial conclusions. Looking back, I must chuckle :-)


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