Influences of trace metals on biological evolution

Scientists show how trace metal chemistry and global changes in oxygen have influenced the evolution of metalloproteins and the Eukaryotes

A paper is being published in PNAS this week about how the varying abundance of trace metals in the environment has influenced biological evolution. The research team, led by Chris Dupont of the J. Craig Venter Institute and Gustavo Caetano-Anollés at the University of Illinois, correlated environmental changes in metal availability over the past 3 billion years ago with the critical events in the evolution of the three superkingdoms of life (Archaea, Bacteria, and Eukaryota).

Billions of years ago, ocean chemistry was dramatically different from today. Completely devoid of oxygen, trace elements such as iron, manganese, and cobalt were abundant. The evolution of photosynthesis resulted in an increase in atmospheric oxygen around 2.4 billion years ago and prompted a series of chemical changes. Over the next 2 billions years the ocean slowly started to accumulate oxygen, increasing the amount of zinc, copper, and molybdenum that was available. At the same time, iron became very rare.

Nearly all biological pathways require metalloproteins (enzymes that bind metals) that are critical for cellular function. The metals utilized by biological life include: Mg, K, Ca, Fe, Mn, Zn, Cu, Mo, Ni, Se, and Co, yet the utilization of these elements varies between organisms. Of these, Fe, Zn, and Ca are the most utilized. Early life, the authors said, lacked both the structures required to control intracellular metal concentrations and the metal-binding proteins themselves involved in electron transport and redox reactions. Within the timeline of protein structure evolution, the invention of proteins that transport and sense metals coincided with the birth of electron transport, as well as the first unique cells. Essentially, the ability to control intracellular metal concentrations appears to be one of the fundamental definitions of biological life.

The first organisms predominantly used metals that were abundant in the ancient ocean, Fe, Mn, and Co. This bias in utilization is preserved to this day in the Bacteria and Archaea, who still predominantly use ancient protein structures. Later, as the ocean accumulated oxygen, new proteins evolved that bound zinc and copper. So did the Eukaryotic superkingdom, which includes all organisms with a nucleus, from single-cell plankton to humans. The authors found that the new zinc and copper-binding proteins are only found in Eukaryotes, not in the Bacteria and Archaea. The nucleus houses most of the new zinc binding proteins and this unique utilization of zinc is one of the defining features of all Eukaryotes. One speculation advanced by the authors is that zinc concentrations in the ancient ocean were too low to allow for the evolution of the Eukaryotes, at least until global changes in oxygen occurred.

This work was funded by the NASA Astrobiology Institute and Dr. Dupont is a collaborator at the “Follow the Elements” NAI institute at Arizona State University. Co-authors on the study include Andrew Butcher from the University of York (UK) and Ruben Valas and Dr. Phil Bourne at the University of California, San Diego.