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Life at the metabolic edge

September 26, 2010

One of the coolest things about microbes from an environmental perspective is the variety of ways they can make a living.  By that I mean how over evolutionary time microbes have evolved an overwhelming diversity of metabolic pathways.

The study I want to tell you about today requires a good deal of background, but I will try to keep it as concise as possible.

Our cells (and those of all animals) use oxygen to convert carbohydrates into carbon dioxide and water, and in the process generate usable energy in the form of ATP molecules.  This is referred to as aerobic cellular respiration, or oxidative metabolism.  If there is not enough oxygen around we can switch things up slightly, for a while, making a little bit of ATP through anaerobic fermentation (which does not require oxygen) but we generate lactic acid (think runners cramps) in the process which our body needs to break down later.

Metabolism in microbes refers not to one reaction with a single variation, but to a suite of reactions, both aerobic and anaerobic, that take advantage of wildly different energy sources.  Many individual microbes can perform a variety of these reactions depending on what chemicals are available to them.  Basically these metabolisms boil down to taking electrons from one compound with a high energy potential, using them to generate usable energy for the cell, and dumping the “used” electrons (now at a lower energy level) on to some other compound that will take them away so that the process can happen over again.

We can measure the reduction potential of a chemical substrate to see how well it acquires electrons or its oxidation potential to see how readily it would give up electrons.  Together these processes are referred to “redox” (as in reduction-oxidation).  As many professors have drilled into my head – life is redox!  Much of the complexity of which microbes do which type of metabolism can be understood simply by knowing the redox potentials of the various electron donors and acceptors available to them.

Each metabolic pathway needs an electron donor and an electron acceptor, and different pairs of chemical will make more or less energy available to a cell based on the difference in redox potential between them.  This amount of free energy in each substrate can be calculated, and the difference between them indicates how much energy will be available to the cell using the pair as its electron donor and acceptor.  Typically this is talked about as Gibbs Free Energy.  For a long time it was assumed that as long as an electron donor/acceptor pair had a change in Gibbs Free Energy of -32 kilojoules per mole some microbe would be able to use that pair of chemicals to generate enough usable energy to live on.  This value based on theoretical thermodynamic calculations of the amount of energy needed for basic cellular processes.  Anything below the magic number of -32 was not thought possible.  That is… until it was discovered that if certain organisms paired up and one’s electron acceptor was immediately used as the other’s electron donor they could each perform an unfavorable metabolism, but the two metabolisms considered together were favorable.  Microbiologists call this type of association syntrophy, and it typically involves hydrogen produced by one species being used by another.

OK, enough background.  Thanks for bearing with me.  Now on to what I really wanted to share…

Earlier this month, it was reported in Nature that a process not generally considered energetic enough to support growth of a single culture of microbes actually is!  The production of bicarbonate and hydrogen (H2) from formate and water had previously been shown in a syntropy between an organism in the genus Morella and one in the genus Methanotherobacter.  The understanding was that Morella wouldn’t be able to grow on formate without Methanobacter to consume the hydrogen that Morella produced, in effect getting it out of the way (in terms of chemical partial pressures) so that the formate reaction would actually be favorable.  However, it had not been shown (until now!) that a single strain of archaea could survive on this formate reaction solo.  The change Gibbs Free Energy for this reaction was calculated to be as low as -8.  How, exactly this organism is able to produce enough ATP to grow, is still not completely worked out.  However, because the whole genome of the organism has been sequenced, scientists will probably be able to determine the detailed mechanisms soon.

The paper that reported this finding is called “Formate-driven growth couple with H2 production”.  The wonder-bug found capable of this simple, yet surprising, anaerobic metabolism is called Thermococcus onnurineus.  It just happens to be one of my favorite types of microbe, a deep sea hydrothermal vent hyperthermophile (this one from the Mid-Atlantic Ridge), meaning that its optimum growth is above 80 degrees celcius!  It is in extreme environments like hydrothermal vents, that these unique strategies might provide organisms with competitive advantages.  In other, more tame, environments other organisms able to carry out more energetically favorable metabolism would simply out compete this microbe.

While this finding might not at first appear thrilling, the discovery that microbes are capable of living off much less energy that we thought was possible leaves me thinking the following things:

  • We really don’t know what the energetic limits of life on earth are.
  • Microbial strategies to eeking out a living are amazing and continue to surprise us.
  • Hydrothermal vents are a great place to find microbes doing things at the extreme limits of what we believe possible.
  • What else might microbes be doing that we are unaware of, and how might those processes be affecting ecosystem function or the environment as a whole?
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