PERSPECTIVES
MICROBIOLOGY
Feasting on Minerals
Dianne K. Newman
F
ar up in the Chilean
Andes, in remote arid
regions seemingly inhos-
pitable to life, intrepid microor-
ganisms thrive on a diet of rocks
and air. Unfazed by long periods
of desiccation or high ultraviolet
energy flux, they grow in baths
of sulfuric acid replete with toxic
metals. The microbes fix carbon
dioxide into biomass by exploit-
ing the energy to be gained by
“eating” (oxidizing) minerals
that contain reduced forms of
iron and sulfur, such as chalco-
pyrite (CuFeS2). Through their
metabolism, these microbes
mobilize precious metals from
ore deposits into solution, making them
powerful catalysts for biomining (see
the first figure) (1). Recent research has
begun to elucidate how they achieve this
remarkable feat.
The Atacama Desert is one of the most
extreme environments on Earth where one
can find mineral-eating microorganisms, but
it is far from the only place where they live.
Bacteria and archaea that grow by oxidizing
ferrous iron, Fe(II), have been found in habi-
tats ranging from the deep sea (2) and acid
mines (3) to wetlands (4), groundwater (5),
and lakes (6). Their metabolic activities can
alter the geochemistry of their surroundings,
influencing the weathering of minerals and
CREDIT: (TOP) IMAGES; PILAR PARADA, NAYIBE BARRETO, AND VERÓNICA GAUTIER/BIOSIGMA
the cycling of major and minor elements.
Some mineral-eating organisms catalyze
mineral oxidation by harnessing energy from
the Sun, others perform this feat in the dark;
some only thrive at pH ~1, others at pH near
7; some require oxygen for their metabolism,
others subsist strictly in its absence (7). But
they all produce ferric iron, Fe(III), as a met-
abolic waste product, which, in many cases,
rapidly precipitates and encrusts the cells.
Other bacteria use these Fe(III) mineral prod-
ucts as terminal electron acceptors for respi-
ration, like humans use oxygen. Yet for the
cells that produce them, they pose something
of a gastronomic hazard—the equivalent of
choking on one’s own meal.
In the past decade, much progress has been
Department of Biology, Massachusetts Institute of Technol-
ogy, Cambridge, MA 02142, USA. E-mail: dkn@mit.edu
www.sciencemag.org SCIENCE VOL 327 12 FEBRUARY 2010
Molecular studies are elucidating how microbes
can eat iron-containing rocks, but many
questions remain.
Unusual diet. The bioleaching pile from the Andina
copper mine in Saladillo, Chile, contains ~60,000
tons of ore (mainly chalcopyrite). Microorganism
such as Acidithiobacillus ferrooxidans inhabit these
piles and catalyze the leaching of precious metals.
The scanning electron micrograph (inset) shows the
cells, 1 to 2 µm in length, attached to a chalcopy-
rite particle.
chemical studies of the acidophile Acidi-
thiobacillus ferrooxidans (see the first figure,
Downloaded from www.sciencemag.org on March 11, 2010
inset) (10), first described almost 60 years
ago (11). More recently, molecular experi-
ments with various model Fe(II)-oxidizing
microorganisms (12–16) have identified spe-
cific electron carriers such as c-type cyto-
chromes (proteins that covalently coordinate
Acidithiobacillus
ferrooxidans heme groups) that appear to be responsible for
delivering electrons from Fe(II) to the respi-
made in understand- ratory chain. These studies have led to a car-
ing how bacteria respire toon-level understanding of the bioenergetic
Fe(III) minerals, that is, pathways in this process (see the second fig-
how they use them as elec- ure) (10), but many details remain obscure.
tron acceptors (8), but much For example, how do mineral eaters con-
less is understood at the molecu- trol their diets? The oxidation substrate,
lar level about how bacteria eat Fe(II) minerals, Fe(II), can be a potent toxin in the presence of
that is, how they use them as electron donors. oxygen, generating reactive oxygen species.
Mineral-eating bacteria are challenging to But even under anaerobic conditions, Fe(II)
cultivate and manipulate in the laboratory can be toxic for certain species. The molecu-
because of their unusual growth constraints, lar basis of this toxicity is unknown, but at
such as extremely acidic pH or a requirement least one bacterium appears to use Fe(II) oxi-
for trace amounts of oxygen (9). However, it dation to detoxify rather than to grow (17).
can be done, and recent studies have begun to Furthermore, all Fe(II) oxidizers require
shed light on their biochemistry. trace quantities of iron to support the biosyn-
Most of what we know comes from bio- thesis of metabolic cofactors. How do they
Iron mineral 2Fe2+ 2Fe3+
OUTER
MEMBRANE pH 2.0
H+ H+ H+ H+
INNER
MEMBRANE
Q
QH2
bc1 aa3 CtaTAB ATPase
NDH1
NAD+ + H+ NADH 2H+ + 1/2 O2 H2O ADP+ Pi ATP
Electron transfer in Acidithiobacillus ferrooxidans. Fe(II) is oxidized to Fe(III) by proteins on the cell sur-
face. These proteins transfer electrons from Fe(II) to other parts of the respiratory chain, leading to the gener-
ation of an energized membrane in the cell. This energy is used to generate metabolites necessary for growth
and other cellular functions. ATP, adenosine 5′-triphosphate; ADP, adenosine 5′-diphosphate; NADH, nicotin-
amide adenine dinucleotide; NADPH, NAD phosphate; NDH1, NADPH dehydrogenase; bc1 complex, ubiqui-
nol-cytochrome c reductase; aa3, cytochrome oxidase; CtaTAB, likely involved in heme sythesis and export to
cytochrome oxidase; ATPase, an enzyme that catalyzes the decomposition of ATP into ADP and phosphate.
793
Published by AAAS
PERSPECTIVES
juggle this demand with that for much larger
amounts of iron for energy generation? And
how do they transport Fe(II) into and Fe(III)
out of the cell? Putative iron transporters have
been identified (12), but little is known about
how they work.
It is becoming clear, however, that min-
eral eaters have a range of gastronomic strat-
egies. Acidophiles circumvent the iron trans-
port issue (at least for growth purposes) by
displaying their Fe(II)-oxidizing enzymes on
their surface (10) and catalyzing Fe(III) min-
eral formation on organic fibrils that extend
away from the cell (18). In contrast, some
neutrophilic Fe(II) oxidizers appear to local-
ize their Fe(II)-oxidizing machinery inside
their cells (12, 13); in some cases, Fe(III)
oxides form in the cells (19), in others outside
(20). What explains the difference?
Microorganisms have a dazzling com-
mand over their intracellular organization
(21), so the localization of their metabolic
machinery cannot be random. It may be that
the way iron presents itself to the cell varies
according to the niche different mineral-eaters
occupy. Furthermore, mineral-eating organ-
isms differ in the complexity of their internal
membrane structures, which may affect their
strategy for electron transfer. Another factor
CHEMISTRY
Radical Ligands Confer Nobility
on Base-Metal Catalysts
Paul J. Chirik1 and Karl Wieghardt2
T
he industrial preparation of many
chemicals relies on the unparalleled
rate and selectivity enhancements
offered by metal compounds in solution. In
many cases, the best catalysts rely on the
scarcest elements, such as rhodium, iridium,
and platinum. The cost of these materials has
long driven efforts to make soluble catalysts
out of cheaper, more Earth-abundant metals
(1), often by modifying their reactivity with
their surrounding ligands. This is especially
true for catalyzing reduction-oxidation, or
redox, reactions, which are critical not only
in catalysis but in energy generation and stor-
age. Such reactions usually change the oxida-
1
Department of Chemistry and Chemical Biology, Cornell
University, Ithaca, NY 14853, USA. 2Max-Planck Institute
for Bioinorganic Chemistry, Stiftstrasse 34-36, D-45470
Mülheim an der Ruhr, Germany. E-mail: pc92@cornell.edu;
wieghardt@mpi-muelheim.mpg.de
794 12 FEBRUARY 2010 VOL 327 SCIENCE www.sciencemag.org
will be whether an organism can produce
Fe(III)-binding molecules or polymers to pre-
vent iron from precipitating internally.
The electron transport machinery in min-
eral-eating organisms also deserves atten-
tion. c-type cytochromes appear to be impor-
tant players in the electron transport chains
of all mineral-eating organisms, but they dif-
fer widely in size and composition. What is
the extent of their diversity? Why do some
organisms use Fe(II) oxidases with 10 hemes,
whereas others require far fewer? How do
these enzymes compare to those of their
respiring counterparts that convert Fe(III) to
Fe(II)? How are they distributed in the cell?
The more we know about how microbes
eat minerals, the better we will understand
the roles these organisms have played and
still play in shaping the geochemistry of
many environments on Earth. These insights
will also help in harnessing their remarkable
metabolisms for industrial applications.
References and Notes
1. C. A. Jerez, in Advances in Applied Bioremediation, A.
Singh, R. C. Kuhad, O. P. Ward, Eds. (Springer, Berlin,
2009), pp. 239–256.
2. B. M. Toner et al., Geochim. Cosmochim. Acta 73, 388
(2009).
3. P. Wilmes et al., ISME J. 3, 266 (2009).
4. J. V. Weiss et al., Geomicrobiol. J. 24, 559 (2007).
tion state of the metal in solution. We discuss
why there can be advantages to having the
redox changes occur in the ligands instead.
One major obstacle in replacing noble
metals with more common ones stems from
the differences in electronic structure. A
noble metal like platinum often favors two-
electron redox changes to promote bond-
making and breaking events. For the base
metals, one-electron redox changes occur
more frequently and present challenges for
controlling reactivity and stabilizing or main-
taining the function of the catalyst.
To mimic noble metals, one-electron redox
changes must be suppressed and two-electron
redox events facilitated. Most ligands used in
inorganic chemistry, such as ammonia or tri-
phenylphosphine, are not “redox-active”—
the energy needed to oxidize or reduce them
by even one electron is much greater than
Published by AAAS
5. M. Blothe, E. E. Roden, Appl. Environ. Microbiol. 75, 468
(2009).
6. S. A. Crowe et al., Proc. Natl. Acad. Sci. U.S.A. 105,
15938 (2008).
7. K. A. Weber, L. A. Achenbach, J. D. Coates, Nat. Rev.
Microbiol. 4, 752 (2006).
8. L. Shi, T. C. Squier, J. M. Zachara, J. K. Fredrickson, Mol.
Microbiol. 65, 12 (2007).
9. G. K. Druschel, D. Emerson, R. Sutka, P. Suchecki, G. W.
Luther, Geochim. Cosmochim. Acta 72, 3358 (2008).
10. R. Quatrini et al., BMC Genomics 10, 394 (2009).
11. K. L. Temple, A. R. Colmer, J. Bacteriol. 62, 605 (1951).
12. Y. Jiao, D. K. Newman, J. Bacteriol. 189, 1765 (2007).
13. L. R. Croal, Y. Q. Jiao, D. K. Newman, J. Bacteriol. 189,
1774 (2007).
14. K. S. Auernik, R. M. Kelly, Appl. Environ. Microbiol. 74,
7723 (2008).
15. S. Bathe, P. R. Norris, Appl. Environ. Microbiol. 73, 2491
(2007).
16. S. W. Singer et al., Appl. Environ. Microbiol. 74, 4454
(2008).
17. A. J. Poulain, D. K. Newman, Appl. Environ. Microbiol.
Downloaded from www.sciencemag.org on March 11, 2010
75, 6639 (2009).
18. C. S. Chan et al., Science 303, 1656 (2004).
19. J. Miot et al., Geochim. Cosmochim. Acta 73, 696 (2009).
20. J. Miot et al., Appl. Environ. Microbiol. 75, 5586 (2009).
21. L. Shapiro, H. H. McAdams, R. Losick, Science 326, 1225
(2009).
22. The author is an investigator of the Howard Hughes Medi-
cal Institute, which has supported her laboratory’s research
on Fe(II) oxidation together with the Dreyfus Foundation
and the NSF. The author thanks A. Poulain, J. D. Newman,
and J. Peters for comments on the manuscript, and A. Bose
for help in preparing the second figure.
10.1126/science.1184229
The oxidation state of metals such as copper
and iron can be stabilized by organic ligands
that add or lose electrons and facilitate catalysis.
that needed to change the oxidation state of
the metal, so changes in electronic structure
occur at the metal. Redox-active, or “non-
innocent,” ligands (2, 3) have more energeti-
cally accessible levels that allow redox reac-
tions to change their charge state. For exam-
ple, NO may bind as a cation in a linear geom-
etry or an anion with a bent geometry.
Redox-active ligands have long been rec-
ognized in coordination chemistry. Gray and
co-workers determined that square-planar
cobalt (4) and nickel (5) dithiolene complexes
were best described as metal(II) compounds
with two ligand radical anions, rather than the
metal in the +4 oxidation state and –2 ligands.
Catecholates and diimines also have a dis-
tinctive ability to form radical species, which
normally would be unstable in solution, when
they are bound to metal centers. The extended
network of π bonds in these ligands allow