Science - USA (2020-08-21)

SCIENCE sciencemag.org 21 AUGUST 2020 • VOL 369 ISSUE 6506 903

battle pollution and power electronic devices

(see sidebar, p. 904). “We are seeing way more

interactions within microbes and between

microbes being done by electricity,” Meysman

says. “I call it the electrical biosphere.”

MOST CELLS THRIVE by robbing electrons

from one molecule, a process called oxida-

tion, and donating them to another mol-

ecule, usually oxygen—so-called reduction.

Energy harvested from these reactions

drives the other processes of life. In eukary-

otic cells, including our own, such “redox”

reactions take place on the inner membrane

of the mitochondria, and the distances in-

volved are tiny—just micrometers. That is

why so many researchers were skeptical

of Nielsen’s claim that cable bacteria were

moving electrons across a span of mud

equivalent to the width of a golf ball.

The vanishing hydrogen sulfide was key

to proving it. Bacteria produce the com-

pound in mud by breaking down plant de-

bris and other organic material; in deeper

sediments, hydrogen sulfide builds up be-

cause there is little oxygen to help other

bacteria break it down. Yet, in Nielsen’s lab-

oratory beakers, the hydrogen sulfide was

disappearing anyway. Moreover, a rusty hue

appeared on the mud’s surface, indicating

that an iron oxide had formed.

One night, waking from his sleep, Nielsen

came up with a bizarre explanation: What if

bacteria buried in the mud were completing

the redox reaction by somehow bypassing

the oxygen-poor layers? What if, instead,

they used the ample supplies of hydrogen

sulfide as an electron donor, then shuttled

the electrons upward to the oxygen-rich

surface? There, the oxidation process would

produce rust if iron was present.

Finding what was carrying these electrons

proved complicated. First, Nils Risgaard-

Petersen on Nielsen’s team had to rule out a

simpler possibility: that metallic particles in

the sediment were shuttling electrons to the

surface and causing the oxidation. He ac-

complished that by inserting a layer of glass

beads, which don’t conduct electricity, into

a column of mud. Despite that obstacle, the

researchers still detected an electric current

moving through the mud, suggesting metal-

lic particles were not the conductor.

To see whether some kind of cable or wire

was ferrying electrons, the researchers next

used a tungsten wire to make a horizontal

slice through a column of mud. The current

flickered out, as if a wire had been snipped.

Other work narrowed down the conductor’s

size, suggesting it had to be at least 1 micro-

meter in diameter. “That’s the conventional

size for bacteria,” Nielsen says.

Ultimately, electron micrographs re-

vealed a likely candidate: long, thin, bac-

terial filaments that appeared in the layer

of glass beads inserted in the beakers filled

with the Aarhus Harbor mud. Each fila-

ment was composed of a stack of cells—up

to 2000—encased in a ridged outer mem-

brane. In the space between that membrane

and the stacked cells, many parallel “wires”

stretched the length of the filament. The

cablelike appearance inspired the microbe’s

common name.

Meysman, the one-time skeptic, quickly

became a convert. Not long after Nielsen

announced his discovery, Meysman decided

to examine one of his own marine mud

samples. “I noticed the same color changes

in the sediment that he saw,” Meysman re-

calls. “It was an instruction from Mother

Nature to take this more seriously.”

His team began to develop tools and tech-

niques for investigating the microbes, some-

times working collaboratively with Nielsen’s

group. It was tough going. The bacterial

filaments tended to degrade quickly once

isolated, and standard electrodes for mea-

suring currents in small conductors didn’t

work. But once the researchers learned how

to pick out a single filament and quickly at-

tach a customized electrode, “We saw really

high conductivity,” Meysman says. The liv-

ing cables don’t rival copper wires, he says,

Hydrogen sulfde

Oxygen (O 2 )

O 2

e–

e–

e–

e–

e–

e–

O 2

e–

e–

e–

e–

OX I DAT I O N

REDUCTION

ELECTRON TRANSFER

Acetate Carbon dioxide +e–

Electrons travel along

nanowires or bacterial cables.

Sulfde Sulfate +e–

+ Hydrogen

Fe+3 Fe+2

Water

Reactions such as

Reactions such as

free up electrons.

1

2

3

e–

1 cm^2

1

3

1

(^23)
Littorella
unifora
Water
Protein wire
Bacterium
Wire
Bacterium
Iron oxide (Fe+3))))
NEWS | FEATURES | MUD
Mud’s electric microbes
At least two kinds of bacteria have evolved electric solutions to gaining energy. These microbes, first discovered
in mud, separate the reduction and oxidation reactions that release the energy needed to fuel life. To enable
these reactions, nanowire bacteria move electrons just micrometers between cells, particles, or other electron
acceptors. Cable bacteria move electrons farther: up to 5 centimeters to oxygen-rich sediments.
A challenging
environment
In ocean and freshwater
sediments, the oxygen
needed for metabolism
is typically restricted
to surface layers or near
plant roots. In deeper
layers, toxic hydrogen
sulfide accumulates as
organic matter decays.
Nanowire bacteria
Found almost
everywhere
microbiologists
have looked, these
bacteria shuttle
electrons gained
through oxidation of
organic compounds
along protein
nanowires to
electron-accepting
substances or cells.
Sometimes these
wires are used
to grab electrons
instead.
Cable bacteria
These bacteria
create a cylinder
of conducting
wires that encases
a chain of cells.
The wires enable
the microbes to
transfer electrons
gained by oxidizing
hydrogen sulfide
to oxygen-rich
sediment, where
the electrons are
used to make water.
GRAPHIC: V. ALTOUNIAN/
SCIENCE
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