Great Balls of Evolution

One organism's trash is another organism's treasure. Our cellular wastes, carbon dioxide and water, nourish plants, which with added energy from sunlight produce the oxygen and sugars that we need to survive. At microscopic scales, these cycles of waste and food can get much more complicated, with many species of microbes working together to survive in harsh environments with limited nutrients.

When organisms (like us) digest sugars made of carbon (C), hydrogen (H), and oxygen (O), they split them up into carbon dioxide (CO2), hydrogen ions (H+) and high-energy electrons (e-) that were holding the energy-dense sugar molecule together. When oxygen is present in the environment, the hydrogen ions and electrons can bind to it, producing water (H2O) and getting a lot of the energy out of the electrons along the way. When there isn't any oxygen around, the cells have a few other options--they can use the electrons to produce lactic acid, like our muscle cells do when they're overworked and use up the available oxygen too fast, or ethanol, like the yeasts used to ferment alcoholic beverages. Some specialized bacteria can transfer the electrons once they're finished with them to metals through specialized structures on the cell surface, creating current in a microbial fuel cell as a byproduct of their natural metabolism. In other species that live almost entirely without oxygen, the hydrogen ions and electrons bind to each other, producing hydrogen gas (H2).

Hydrogen still has a lot of energy trapped inside it, which is why it might be a good fuel and why it's not a very good waste product. A bacterium producing hydrogen is losing a lot of energy it could have gotten from those electrons, and when too much hydrogen is present in the environment the cell's metabolism slows down and it gets even harder to squeeze out any energy. Other bacteria living in close proximity to these hydrogen producers can use that energy, taking the carbon dioxide and hydrogen waste and turning it into methane (CH4, a.k.a. natural gas, is another possibly sustainable fuel when produced by microbes) and water. Neither cell in this arrangement can live without the other; the hydrogen producer would suffocate on it's own waste without the hydrogen consumer, and the methane producer would starve without the hydrogen producer because it can't break down the more complex molecules that the hydrogen producer can digest. Because this hydrogen transfer is required for both cells to survive, the sharing species will clump together into cell aggregates visible to the naked eye, so that hydrogen can travel more efficiently from the producer to the consumer. Some hypothesize that aggregates such as these may have been the basis for the evolution of the first eukaryotic cells.

This aggregate-forming interspecies hydrogen transfer has been known and studied for decades, but recently, researchers in Derek Lovley's lab at UMass Amherst sought to better understand how such aggregates can evolve through an artificial evolution experiment. They mixed together two species of Geobacter, one that can break down ethanol into carbon dioxide and hydrogen to get energy, and one that can't break down ethanol but can use the energy from hydrogen to grow. As Lovley explains, "They're the ultimate drinking buddies, collaborating to consume ethanol."

Geobacter are really good at transferring their electrons through conductive structures on their surface called pili to metals and other inorganic substrates, and can make a small but appreciable amount of electricity in microbial fuel cells. In this experiment they didn't have any metals to put their electrons on, they had to produce hydrogen or they would die. The mixed cultures grew very slowly at first as they switched to this more difficult metabolism, but after a few months they were able to digest 70% of the ethanol in the starting culture, at which time the researchers transferred the cells to fresh ethanol. This time, the cells ate 70% of the ethanol much faster, and after a few such transfers they found that the cells were forming aggregates like those found in nature that had evolved over the course of a few months to be much more efficient sharers--great balls of evolution.

But that's not the whole story. To make sure that the aggregates that were forming and growing were actually sharing hydrogen, they deleted the enzyme that allows the consumer to eat hydrogen, expecting the cell mixture to never be able to grow. Instead, they found that the aggregates evolved much faster than before, in 21 days instead of 7 months!

When they sequenced the DNA of the evolved hydrogen consumer they found just one change from the wild type strain, in a gene that controls the activity of many other genes. While the expression of many genes is affected by such a mutation, facilitating large-scale evolution, one gene in particular was affected--OmcS, a gene that controls the transfer of electrons down the conductive pili. The mutation in the control gene allowed for higher expression of OmcS, and a higher ability to transfer electrons directly from outside the cell. The over-expression of these iron-rich proteins also explained the bright red color of the evolved aggregates. But without any inorganic substrates, there was only one explanation for where the electrons were going--the pili were conducting electrons directly from one species to the other, without any need for hydrogen as an intermediate.

I love this paper because it shows both how diverse and stingy bacterial metabolism is and how amazingly complex cooperative behaviors can evolve rapidly with the right selective pressures. In conclusion, cooperation + metabolism + hydrogen + electricity + evolution = AWESOME.

via molecularist

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Zarath M. Summers et. al. (2010) Direct Exchange of Electrons With Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria. Science 330:6009, 1413-1415.