An Overlooked Opportunity to Breath Without Oxygen

An Overlooked Opportunity to Breath Without Oxygen
Pure Manganese III oxide powder, an electron acceptor.

Unlike humans, who depend on oxygen to breathe, bacteria have the ability to breathe many other molecules besides oxygen. While most of our Earth is soaked in oxygen, there are areas that have little to none. In sediments at the bottom of lakes, oceans and marshes, oxygen is consumed rapidly within few centimeters below the top so bacteria that can breathe other substrates can shift between using oxygen, to using nitrate, or sulfate, or manganese oxides. The benefit for them is that by not depending on just one of these molecules, they can survive in a greater variety of environments. These other molecules that bacteria breathe (oxygen, nitrate, sulfate, and manganese oxides) are called electron acceptors because the high-energy electrons in food jump to these molecules and in the process release energy that can be used by the cells to grow, move and divide.

We care about organisms that can do this because they keep carbon and nutrients flowing in environments where there is no oxygen. Among these electron acceptors, manganese is important, has a unique property. Manganese oxides do not dissolve in water, and since cells are mostly water surrounded by a lipid (oily) membrane, it is difficult for bacteria to get manganese inside to respire on it, like they do with other acceptors. So how can bacteria breathe on these rocks?

If the mountain cannot come to the electron, they bring the electron to the mountain. Manganese-breathing bacteria have molecules that act as wires, to carry the electrons outside, where manganese is. This is very different that what our cells do. We just keep it indoors. When the electrons jump onto manganese, the manganese dissolves in water. This is very important, because photosynthesis depends on dissolved (reduced) manganese.

In the environment, there is a third form of manganese that has been hiding from the scientific community for a while: Manangese (III). Mn(III) can be found as a solid or dissolved. Scientist developed a method to measure it, and found a surprisingly high amount of manganese III in the ocean just below where oxygen disappears. Bacteria are important for converting between the different forms of manganese because these reactions are very slow on their own. Can bacteria use Mn(III) as they do Mn(IV)? If they do, this means that Mn(III) is another electron acceptor that scientists have not accounted for.

A single Shewanella algae cell. Source: MicrobeWiki

Researchers at Georgia Tech set out to answer this question by growing a sample of bacteria from the environment on a common food source, acetate, in an oxygen-free environment with only manganese III as the electron acceptor. The results showed that the bacteria were definitely breathing manganese III. Over time, from the whole pool of microbes sampled from the environment, a strain called Shewanella was the most abundant and appeared to have outcompeted the rest. The researchers were puzzled. Their lab had been working with Shewanella strains for over 15 years, and they did not expect to get one growing with acetate. Shewanella are known for their capacity to use acetate only when there is oxygen, but not without.

Scientists have been studying Shewanella for more than 30 years, and have figured out what they like to grow in, what they can use as food, and most thoroughly, how they reduce (take electrons from) metals. Most studies with Shewanella use lactate as their food source under oxygen-free conditions. With lactate, Shewanella can reduce manganese.

But this Shewanella was different. A test in which acetate was tagged for tracking showed that this strain was oxidizing acetate without a doubt, using manganese III as the electron acceptor!

The incubations and isolated microorganisms showed that Mn(III) can be used as an electron acceptor with acetate. This result is exciting because it means that bacteria can survive in environments without oxygen, if there is manganese III. It opens the door to more research into what other species of microbes breathe manganese III.

Acetate is a very simple food source, and possibly one of the first food sources that were available on Earth for the first bacteria that lived on the planet. Bacteria came before photosynthesis, so they lived without oxygen. Understanding how bacteria can use acetate with other electron acceptors, like Manganese III, brings us closer to understanding how life appeared and changed in our planet.

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