Microbes care about energy efficiency

by Adityarup "Rup" Chakravorty
Friday, October 13, 2017

Microbes live in some of the most extreme environments on Earth, from the crushing depths of deep-sea trenches to scalding geothermal springs. Part of the reason microbes thrive in many different environments is their ability to use a variety of energy sources — including light, organic matter, and inorganic materials like hydrogen, sulfur, and iron — to power the metabolic reactions that allow them to grow and survive.

Researchers have typically assumed that microbes, given a choice, would prefer energy sources, or substrates, that yield more energy over those that yield less. But in a new study in Nature Geoscience, scientists found that, in some environments, microbes may select easier-to-metabolize substrates that yield less energy over substrates that yield more energy but are more demanding to process.

“Imagine you are gearing up for a marathon; you want to load up on simple carbohydrates and not a lot of complex fatty foods [even though fats contain more energy per gram], because carbohydrates are easier to break down,” says Eric Boyd, a microbiologist at Montana State University and lead author of the new study. “It’s a similar concept for microbial cells.”

All organisms metabolize substrates to generate energy, often through series, or chains, of electron transport reactions in which electrons are transferred from donor molecules to acceptor molecules.

Members of the heat-loving archaeal genus Acidianus can use either hydrogen gas (H2) or elemental sulfur (S) as electron donors, and either sulfur or ferric iron (Fe3+) as electron acceptors in their metabolisms. Boyd and his colleagues tested which of three different donor-acceptor pairs — H2/S, H2/Fe3+ or S/Fe3+ — was preferred by a strain of Acidianus isolated from a hot spring in Yellowstone National Park.

Thermodynamic calculations indicated that the H2/Fe3+ and S/Fe3+ pairs would yield three- and four-fold more energy, respectively, compared to the H2/S couple. Yet, when the researchers provided Acidianus cells with all three substrate pairs at the same time, the archaeon preferred to use the H2/S pair. Also, the Acidianus cells assimilated eight times as much carbon — meaning they grew more efficiently — for the same amount of energy from the H2/S couple compared to either the H2/Fe3+ or S/Fe3+ couples.

That Acidianus cells preferred the substrate pair that yields the least energy runs counter to the prevailing idea about microbial substrate preferences. The reason, Boyd says, may lie in how efficiently the cells can extract energy using each pair of substrates. “Using the H2/S couple for energy is arguably one of the simplest processes,” he says. “There are only two steps [in the electron transport chain], and it can be very efficient.”

The details of the electron transport chains in Acidianus involving iron as an electron acceptor are not totally clear, but it appears they involve more steps and require more work on the part of the microbes, the researchers reported. This means that the cells have to expend more energy to get energy using iron. Additionally, in a longer electron transfer chain, “just like a high-voltage line, electron transport isn’t 100 percent efficient, so energy would be lost during the transfer process as well,” Boyd says.

The explanation put forward by Boyd and colleagues is reasonable, but there could be other reasons for Acidianus preferring the H2/S couple as an energy source in the laboratory, says William Cannon, a biophysicist at Pacific Northwest National Laboratory in Washington, who wasn’t involved in the study. For example, “in the environmental microbiome from which this strain of Acidianus was isolated … efficient growth [may require] production of some metabolites by partner organisms,” he says. In other words, in their natural environment, Acidianus might get help from its neighbors to use higher-energy substrate pairs efficiently.

The results of this study shouldn’t be interpreted too broadly because it focuses on just one organism, Cannon says, but he adds that “quantitative studies like this one that link physical principles such as thermodynamics to microbial physiology can allow us to make accurate predictions about microbial communities and metabolism.”

That’s an important contribution, Boyd says, because microbes drive biogeochemical cycles and heavily influence the composition of the atmosphere, oceans and soils. So, he says, “better understanding the thermodynamics of microbial activity” will offer an improved picture of “what is happening in these different environments.”