The Terminator. The Borg. The Six Million Dollar Man. Science fiction is ripe
with biological beings armed with artificial capabilities. In reality, however,
the clunky connections between living and non-living worlds often lack a clear
channel for communication.
Now, scientists with the Lawrence
Berkeley National Laboratory (Berkeley Lab) have designed an electrical
link to living cells engineered to shuttle electrons across a cell’s membrane
to an external acceptor along a well-defined path. This direct channel could
yield cells that can read and respond to electronic signals, electronics capable
of self-replication and repair, or efficiently transfer sunlight into electricity.
An engineered Escherichia coli strain (yellow) attaching to solid iron oxide (black). Scientists at the Molecular Foundry took the first step toward electronically interfacing microbes with inorganic materials, without disrupting cell viability. (Image courtesy of Heather Jensen)
“Melding the living and non-living worlds is a canonical image in science
fiction,” said Caroline Ajo-Franklin, a staff scientist in the Biological
Nanostructures Facility at the Molecular Foundry. “However, in most attempts
to interface living and non-living systems, you poke cells with a sharp hard
object, and the cells respond in a predictable way – they die. Yet, in
Nature many organisms have evolved to interact with the rocks and minerals that
are part of their environment. Here, we took inspiration from Nature’s
approach and actually grew the connections out of the cell.”
Coaxing electrons across a cellular membrane is not trivial: attempts to pull
an electron from a cell may disrupt its function, or kill the entire cell in
the process. What’s more, current techniques to transfer cellular electrons
to an external source lack a molecular roadmap, which means even if electrons
do turn up outside a cell, there is no way to direct their behavior, see where
they stopped along the way, or send a signal back to the cell’s interior.
“We were interested in finding a pathway that wouldn’t kill the
living systems we were studying,” said Heather Jensen, a graduate student
at University of California, Berkeley whose thesis work is part of this publication.
“By using a living system in electronics, we can one day create biotechnologies
that can repair and self-replicate.” In their approach, Jensen, Ajo-Franklin
and colleagues first cloned a part of the extracellular electron transfer chain
of Shewanella oneidensis MR-1, marine and soil bacteria capable of reducing
heavy metals in oxygen-free environments. This chain or “genetic cassette,”
Ajo-Franklin notes, is essentially a stretch of DNA that contains the instructions
for making the electron conduit. Additionally, because all life as we know it
uses DNA, the genetic cassette can be plugged into any organism. The team showed
this natural electron pathway could be popped into a (harmless) strain of E.
coli—a versatile model bacteria in biotechnology— to precisely channel
electrons inside a living cell to an inorganic mineral: iron oxide, also known
as rust.
Bacteria in environments without oxygen, such as Shewanella, use iron oxide
from their surroundings to breathe. As a result, these bacteria have evolved
mechanisms for direct charge transfer to inorganic minerals found deep in the
sea or soil. The Berkeley Labs team showed their engineered E. coli could efficiently
reduce iron and iron oxide nanoparticles—the latter five times faster
than E. coli alone.
“This recent breakthrough is part of a larger Department of Energy project
on domesticating life at the cellular and molecular level. By directly interfacing
synthetic devices with living organisms, we can harness the vast capabilities
of life in photo- and chemical energy conversion, chemical synthesis, and self-assembly
and repair,” said Jay Groves, a faculty scientist at Berkeley Labs and
professor of chemistry at University of California, Berkeley. “Cells have
sophisticated ways of transferring electrons and electrical energy. However,
just sticking an electrode into a cell is about as ineffective as sticking your
finger into an electrical outlet when you are hungry. Instead, our strategy
is based on tapping directly into the molecular electron transport chain used
by cells to efficiently capture energy.”
The researchers plan to implement this genetic cassette in photosynthetic bacteria,
as cellular electrons from these bacteria can be produced from sunlight—providing
cheap, self-replicating solar batteries. These metal-reducing bacteria could
also assist in producing pharmaceutical drugs, Ajo-Franklin adds, as the fermentation
step in drug manufacturing requires energy-intensive pumping of oxygen. In contrast,
these engineered bacteria breathe using rust, rather than oxygen, saving energy.
A paper reporting this research titled, “Engineering of a synthetic electron
conduit in living cells,” appears in Proceedings of the National Academy
of Sciences and is available to subscribers online. Co-authoring the paper with
Jensen, Ajo-Franklin and Groves were Aaron Albers, Konstantin Malley, Yuri Londer,
Bruce Cohen, Brett Helms and Peter Weigele.
Portions of this work at the Molecular Foundry were supported by DOE’s
Office of Science.