Environment and sustainability

How bacteria adapted to an oxygen-rich planet 2.5 billion years ago

Rapidly rising levels of oxygen in the Earth’s atmosphere 2.5 billion years ago forced bacteria to adapt to this new and harmful environment. Researchers have now figured out how they did this.

Quinones are involved in respiration. Some microorganisms use two types of quinones to transport electrons within the cells when they need to produce energy. Humans, other animals and plants use only one type, coenzyme Q10, which is sold as a nutraceutical.

For many years, researchers have wondered what evolutionary drivers cause some bacteria to develop two types of quinones, but this has been answered in a new study published in the Proceedings of the National Academy of Sciences of the United States of America.

The study shows that, when oxygen levels in the atmosphere increased dramatically 2.5 billion years ago, these bacteria developed a new type of quinone that protected better against the toxic oxygen that threatened to tear them apart if they used the previous type of quinone.

This new and oxygen-optimized type of quinone has since been transferred to all other living organisms on the planet, including the people living today.

“This is a very neat study that answers a fundamental question that researchers have been asking for many years: Why do most organisms today use ubiquinone instead of naphthoquinone in electron transport? What is the difference between them and what was the advantage of switching?,” says a researcher behind the new study, Bernhard Palsson, CEO, Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Kongens Lyngby.

Bacteria changed the Earth 2.5 billion years ago

Almost all living organisms use ubiquinone in the electron transport chain for converting glucose into energy, water and oxygen.

Before ubiquinone, bacteria and archaea used naphthoquinone, but researchers have not quite understood why the microorganisms switched from using one type of quinone to another.

The answer lies in the distant past.

The ancient primitive bacterial species, cyanobacteria, began to fill the Earth’s atmosphere with toxic oxygen 2.5 billion years ago.

Oxygen leads to oxidative stress at the cellular level because reactive oxygen species can enter and bind to and destroy many proteins and enzymes.

Reactive oxygen inside the cells therefore needs to be constantly monitored, such as throughout the electron transport chain, where there is interaction with various reactive oxygen ions.

“Naphthoquinone tends to release electrons, and when this happens, oxygen can become reactive oxygen species (ROS) that can destroy the cells from within. Ubiquinone, in contrast, is much better at retaining electrons than naphthoquinone, and switching to ubiquinone rather than using naphthoquinone was therefore evolutionarily beneficial to ancient bacteria,” explains Bernhard Palsson.

Divided Escherichia coli into two groups with different quinones

In the study, the researchers studied E. coli bacteria, one of a group of organisms that still use both ubiquinone and naphthoquinone.

E. coli can survive in a very oxygen-poor environment, such as inside people’s intestines, but they can also survive outside the body, where there is plenty of oxygen. The bacteria have therefore retained their ability to switch between the two different types of quinones depending on their environment.

In the study, the researchers knocked out the respective genes for ubiquinone and naphthoquinone production and created two new strains of E. coli whose functions could be compared with those of the wild-type strain.

Then they observed how the bacteria evolved and functioned.

• The group of wild-type bacteria grew as usual.

• The bacteria that use ubiquinone did too.

• In contrast, the bacteria that use naphthoquinone grew 30% slower than the other strains.

“That was our first observation. Ubiquinone-based bacteria grow much faster in today’s oxygen-rich environment than naphthoquinone-based bacteria,” says Bernhard Palsson.

Naphthoquinone-based bacteria need to defend themselves against oxidative stress

The researchers then investigated why the naphthoquinone-based bacteria grew more slowly than the ubiquinone-based bacteria.

The naphthoquinone-based bacteria had to allocate many resources to defend themselves against oxidative stress within the cells and between the cell’s two outer membranes.

This defence includes superoxide dismutase and peroxidase, and the naphthoquinone-based bacteria fill in the space between the cell’s two outer membranes (periplasm), the key location for the electron transport chain.

“The bacteria need to use many resources to protect themselves from these reactive oxygen species that arise in the electron transport chain because naphthoquinone does not bind oxygen well enough. This did not matter 2.5 billion years ago or in another oxygen-poor environment, but it is very important for life in the present atmosphere, which is why the E. coli that can only use naphthoquinone in our experiments grow more slowly,” explains Bernhard Palsson.

Fundamental understanding of biology

Bernhard Palsson explains that replacing naphthoquinone with ubiquinone is not the only initiative the bacteria implemented in their life cycle when oxygen levels began to rise in the atmosphere 2.5 billion years ago.

The researchers are completing a study examining other components of the electron transport chain to see how these are structured.

“This revolves around basic understanding of biology and understanding why cell components look and behave the way they do, and it offers a glimpse into the evolutionary toolbox,” says Bernhard Palsson.

Adaptive evolution reveals a tradeoff between growth rate and oxidative stress during naphthoquinone-based aerobic respiration” has been published in the Proceedings of the National Academy of Sciences of the United States of America. Several authors are employed at the Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, Kongens Lyngby.

Bernhard O. Palsson
Bernhard Palsson is a Distinguished and the Galletti Professor of Bioengineering, Professor of Pediatrics, and the Principal Investigator of the Systems Biology Research Group in the Department of Bioengineering at the University of California, San Diego. Dr. Palsson has co-authored more than 500 peer-reviewed research articles and has authored four textbooks, with more in preparation. He is CEO at the Novo Nordisk Foundation Center for Biosustainability in Denmark. His research includes the development of methods to analyze metabolic dynamics (flux-balance analysis, and modal analysis), and the formulation of complete models of selected cells (the red blood cell, E. coli, CHO cells, and several human pathogens). He sits on the editorial broad of several leading peer-reviewed microbiology, bioengineering, and biotechnology journals. He previously held a faculty position at the University of Michigan for 11 years and was named the G.G. Brown Associate Professor at Michigan in 1989. He is inventor on over 40 U.S. patents, the co-founder of several biotechnology companies, and holds several major biotechnology awards. He received his PhD in Chemical Engineering from the University of Wisconsin, Madison in 1984. Dr. Palsson is a member of the National Academy of Engineering and is a Fellow of both the AAAS and the AAM.