Unveiling the Enigmatic Dual - Respiration of Microbes: Insights into Life's Evolutionary Transition

The original narrative of this study was initially published in Quanta Magazine.

The Duality of Respiration in the Biological Realm

Take a moment to consider the act of respiration. When you inhale deeply, a stream of air floods your lungs. Here, oxygen diffuses into your bloodstream, serving as the catalyst for metabolic processes in cells throughout your body. As an aerobic organism, you rely on oxygen to unlock the molecular energy stored within the food you consume. However, not all life forms on Earth adhere to this oxygen - dependent mode of living. Many single - celled organisms inhabiting oxygen - deprived environments, such as deep - sea hydrothermal vents or dark crevices in the soil, employ alternative elements for respiration and energy extraction.

This segregation between oxygen - rich and oxygen - free habitats is not merely a matter of resource utilization; it is a biochemical imperative. Oxygen is incompatible with the metabolic pathways that enable respiration using elements like sulfur or manganese. While it sustains life for aerobes like us, for many anaerobes—organisms that respire without oxygen—oxygen is a toxic substance that can react with and damage their specialized molecular mechanisms.

Courtney Stairs, an evolutionary biologist at Lund University in Sweden, aptly noted, “Oxygen—we cherish it, of course. But it is, in fact, a rather harmful molecule for most of life on our planet, including ourselves. We have developed means to mitigate its negative impacts. Thus, while we can scarcely fathom life without it, life with it presents its own set of challenges.”

The Great Oxidation Event: A Pivotal Shift in Earth's Biosphere

For the first few billion years of life on Earth, organisms evaded the oxygen conundrum altogether. During this era, the air and oceans were largely oxygen - free, and life was predominantly anaerobic. Then, around 2.7 billion years ago, the seas witnessed the proliferation of industrious, photosynthetic cyanobacteria. These organisms had developed a mechanism to convert sunlight into sugar and oxygen, leading to their flourishing. Over hundreds of millions of years, their cumulative respiration gradually filled the atmosphere and oceans with oxygen. This so - called Great Oxidation Event was a transformative milestone in the biosphere, as well as in the physical chemistry of Earth's atmosphere and oceans. In this new oxygen - rich environment, aerobic respiration evolved to become the dominant mode of life.

One of the enduring mysteries for researchers has been how life navigated the transition from anaerobic to aerobic respiration. Given the vast microbial biodiversity, adapting to a world filled with what was once a biochemical threat was no small feat. Now, researchers have gained novel insights into this ancient transition, thanks to a contemporary organism. A bacterium collected from the cauldron of a Yellowstone National Park hot spring exhibits an extraordinary ability: it simultaneously conducts aerobic and anaerobic metabolisms, breathing both oxygen and sulfur.

Natalia Mrnjavac, a graduate student in evolutionary microbiology at Heinrich Heine University Düsseldorf in Germany, who was not involved in the study, remarked, “The findings once again remind us of how much remains to be discovered regarding microbial diversity and metabolism. And for those of us who are fascinated by microbes, this is truly exhilarating.”

These findings, published earlier this year in Nature Communications, challenge long - held assumptions about the boundaries of cellular respiration and may provide researchers with a model for understanding how life teeters on the brink of a beneficial yet potentially toxic environment.

Metabolic Tricks: Unveiling the Unusual Respiration of Hydrogenobacter RSW1

It has long been recognized that life forms have evolved strategies to alternate between aerobic and anaerobic respiration, often as a survival mechanism when oxygen levels are low. However, due to oxygen's disruptive effect on anaerobic respiration, many researchers assumed that cells could not grow while simultaneously engaging in both processes.

When Eric Boyd, a microbiologist at Montana State University in Bozeman, and his colleagues came across reports from the late 1990s and early 2000s suggesting that some bacteria might be doing precisely that, their curiosity was piqued. Specifically, bacteria had been observed producing sulfide, a by - product of anaerobic respiration, even in the presence of oxygen. Boyd recalled, “Reading something like that is quite strange because it challenges the established knowledge in textbooks regarding microbial metabolism.”

Boyd is intrigued by how life evolves and persists in some of the most chemically and thermally extreme environments on Earth. His team studies the resilient microbes inhabiting the interfaces between the surface and subterranean worlds, including the volcanic vents and thermal pools of Yellowstone National Park, which is in close proximity to his university in Montana. The peculiar microbe that seemingly employed anaerobic respiration even when oxygen was available was a perfect fit for their research interests. To delve deeper into its capabilities, Boyd and his team had to explore the turbulent springs where such a microbe would thrive, areas where volcanic bubbles mix with the oxygen - rich atmosphere and oxygen - free groundwater.

From a roadside thermal spring near Nymph Lake in the northwest part of the park, they collected and isolated a strain named Hydrogenobacter RSW1. RSW1 seemed like an ideal candidate for studying unusual respiration. This bacterium is prevalent in volcanically - influenced hot springs worldwide, from Iceland to New Zealand, and can grow with minimal oxygen. Moreover, it belongs to the same order, Aquificales, as the curious microbes mentioned in the earlier reports. The researchers brought it back to the laboratory to cultivate and analyze its metabolism.

The team systematically determined the elements and molecules on which the bacterial strain could grow. Knowing it could utilize oxygen, they tested various combinations in the lab. In the absence of oxygen, RSW1 could process hydrogen gas and elemental sulfur—substances found in volcanic vent emissions—and produce hydrogen sulfide. However, while the cells remained alive in this state, they did not grow or replicate. They generated only a minimal amount of energy, just enough for survival. Boyd described it as “the cell merely idling without achieving any significant metabolic or biomass gain.”

When the team re - introduced oxygen, the bacteria grew more rapidly, as expected. However, to their surprise, RSW1 continued to produce hydrogen sulfide gas, as if it were still anaerobically respiring. In fact, the bacteria appeared to be breathing both aerobically and anaerobically simultaneously, reaping the energy benefits of both processes. This dual respiration went beyond the earlier reports; the cell was not only producing sulfide in the presence of oxygen but also actively performing both conflicting processes concurrently. Such an ability defied conventional understanding of bacterial capabilities.

Boyd exclaimed, “That set us on a quest to understand, ‘OK, what on earth is really happening here?’”

Breathing Two Ways: The Hybrid Metabolism of RSW1

RSW1 appears to possess a hybrid metabolism, operating an anaerobic sulfur - based mode concurrently with an aerobic oxygen - based mode.

Ranjani Murali, an environmental microbiologist at the University of Nevada, Las Vegas, who was not part of the research, stated, “For an organism to be able to integrate these two metabolisms is truly unique.” She explained that normally, when anaerobic organisms are exposed to oxygen, reactive oxygen compounds, which are damaging molecules, create stress. “The fact that this does not occur in RSW1 is truly fascinating.”

Boyd's team observed that the bacteria grew most optimally when running both metabolisms simultaneously. This may confer an advantage in its unique environment. In hot springs like those where RSW1 resides, oxygen is not uniformly distributed. In constantly changing conditions, where oxygen availability can fluctuate rapidly, having a dual - metabolic strategy could be a highly adaptive trait.

Other microbes have been observed respiring in two ways simultaneously, such as anaerobically with nitrate and aerobically with oxygen. However, these processes utilize entirely different chemical pathways and, when combined, often impose an energetic cost on the microbes. In contrast, RSW1's sulfur/oxygen hybrid metabolism enhances the cells rather than burdening them.

This type of dual respiration may have eluded detection until now because it was considered impossible. Boyd noted, “You have no real incentive to look for something like this.” Additionally, oxygen and sulfide react rapidly with each other. Unless one is specifically monitoring for sulfide as a by - product, it could easily be overlooked.

Murali posited that microbes with dual metabolisms may, in fact, be widespread. She pointed to the numerous habitats and organisms existing at the delicate gradients between oxygen - rich and oxygen - free regions. One example is submerged sediments, which can host cable bacteria. These elongated microbes position themselves in a way that one end of their bodies can engage in aerobic respiration in oxygenated water, while the other end, buried deep in anoxic sediment, uses anaerobic respiration. Cable bacteria thrive in this precarious divide by physically separating their aerobic and anaerobic processes. In contrast, RSW1 appears to multitask while in the turbulent spring.

It remains unknown how RSW1 bacteria safeguard their anaerobic machinery from oxygen. Murali speculated that the cells might form chemical supercomplexes within themselves that can surround, isolate, and “scavenge” oxygen, rapidly consuming it upon encounter to prevent interference with sulfur - based respiration.

Boyd suggested that RSW1 and any other microbes with dual metabolism offer fascinating models for understanding how microbial life may have evolved during the Great Oxygenation Event. He said, “That must have been a highly chaotic period for the planet's microbes.” As oxygen gradually seeped into the atmosphere and sea, any life form that could tolerate occasional exposure to this new, toxic gas—or even harness it for energy—may have had a competitive edge. During this transitional period, having two metabolisms may have been more advantageous than having just one.

Original story reprinted with permission from Quanta Magazine, an editorially independent publication of the Simons Foundation whose mission is to enhance public understanding of science by covering research developments and trends in mathematics and the physical and life sciences.