MINI-REVIEW
Advantages and challenges of increased antimicrobial copper
use and copper mining
Jutta Elguindi & Xiuli Hao & Yanbing Lin &
Hend A. Alwathnani & Gehong Wei &
Christopher Rensing
Received: 5 April 2011 /Revised: 11 May 2011 /Accepted: 11 May 2011 /Published online: 9 June 2011
# Springer-Verlag 2011
Abstract Copper is a highly utilized metal for electrical,
automotive, household objects, and more recently as an
effective antimicrobial surface. Copper-containing solutions
applied to fruits and vegetables can prevent bacterial and
fungal infections. Bacteria, such as Salmonellae and
Cronobacter sakazakii, often found in food contamination,
are rapidly killed on contact with copper alloys. The
antimicrobial effectiveness of copper alloys in the health-
care environment against bacteria causing hospital-acquired
infections such as methicillin-resistant Staphylococcus aureus
(MRSA), Escherichia coli O157:H7, and Clostridium
difficile has been described recently. The use of copper and
copper-containing materials will continue to expand and may
lead to an increase in copper mining and production.
However, the copper mining and manufacturing industry
and the consumer do not necessarily enjoy a favorable
relationship. Open pit mining, copper mine tailings, leaching
products, and deposits of toxic metals in the environment
often raises concerns and sometimes public outrage. In
addition, consumers may fear that copper alloys utilized as
antimicrobial surfaces in food production will lead to copper
toxicity in humans. Therefore, there is a need to mitigate some
of the negative effects of increased copper use and copper
mining. More thermo-tolerant, copper ion-resistant micro-
organisms could improve copper leaching and lessen copper
groundwater contamination. Copper ion-resistant bacteria
associated with plants might be useful in biostabilization and
phytoremediation of copper-contaminated environments. In
this review, recent progress in microbiological and biotech-
nological aspects of microorganisms in contact with copper
will be presented and discussed, exploring their role in the
improvement for the industries involved as well as providing
better environmental outcomes.
Keywords Antimicrobial copper. Copper mining .
Phytoremediation .Microbial copper resistance
Introduction
Copper is an essential micronutrient element required by
almost all living organisms, including humans, as it
contributes to the function of numerous essential metabolic
processes. However, copper ions at increased levels are
toxic to most organisms due to their ability to generate
reactive oxygen species and act as a strong soft metal, e.g.,
leading to a release of iron from Fe–S clusters (Macomber
and Imlay 2009). Copper was the first metal used by human
civilizations, presumably because it could be found in the
native, metallic form which does not require smelting
(Grass et al. 2011). The use of copper needles in ancient
Chinese acupuncture is thought to have originated from the
Yellow Emperor Huang-Ti and was recorded in the Internal
Medical Classic, Nei Ching, around 2500 B.C. (Fields
1947). Copper was also an ingredient in ancient Chinese
mineral preparations (“stone drugs”), which have been
J. Elguindi : X. Hao : Y. Lin : C. Rensing (*)
Department of Soil, Water, and Environmental Science,
University of Arizona,
Shantz Building #38 Rm 429,
Tucson, AZ 85721, USA
e-mail: rensingc@ag.arizona.edu
X. Hao : Y. Lin : G. Wei
College of Life Sciences, Northwest A & F University,
Yangling, Shaanxi 712100, China
H. A. Alwathnani : C. Rensing
College of Science, Department of Botany and Microbiology,
King Saud University,
Riyadh, Saudi Arabia
Appl Microbiol Biotechnol (2011) 91:237–249
DOI 10.1007/s00253-011-3383-3

adapted over the past 2,000 years for treatment of specific
diseases such as endemic fluorosis and Kaschin–Beck
disease (Yu et al. 1995). An Egyptian medical text, written
between 2600 and 2200 B.C., describes the application of
copper to sterilize drinking water and chest wounds. The
ancient Greeks of the pre-Christian era of Hippocrates
(400 B.C.) discovered the sanitizing power of copper
thousands of years ago, and they prescribed copper for
pulmonary diseases and for purifying drinking water
(Dollwet and Sorenson 1985).
However, humans were not the first to discover and
use the antimicrobial properties of copper. Macrophages
in the human and other mammalian immune systems
concentrate copper to enhance killing by oxidative burst
(White et al. 2009). Therefore, pathogens such as
Mycobacterium tuberculosis, Staphylococcus aureus, or
Salmonella enterica serovar Typhimurium able to survive
in macrophages require unique copper resistance systems
(Osman et al. 2010; Soutourina et al. 2010; Wolschendorf
et al. 2011). In contrast, studies have shown that copper
deficiency impaired the bactericidal activity of neutrophils
and macrophages in vitro (Babu and Failla 1990a, b). Rice
plants also appear to derive some protection from copper
in their xylem as pathogens such as Xanthomonas oryzae
pv oryzae need to induce copper redistribution to be able
to proliferate and spread causing bacterial blight disease
(Yuan et al. 2010). This might be a widespread antimicro-
bial mechanism in plants.
Copper also has a great environmental impact. Global
estimates indicate the oceans are responsible for approxi-
mately half of the carbon dioxide fixed on Earth. Marine
cyanobacteria such as Proclorococcus and Synechococcus
as well as small eukaryotic algae are thought to be
responsible for much of the surface water-mediated photo-
synthesis and subsequent CO2 fixation. In a recent paper,
Paytan et al. (2009) reported that Sahara aerosols can
readily inhibit photosynthesis. Copper, a metal that can
inhibit photosynthesis and other cellular functions, is
thought to be a significant component of these aerosols.
Stuart et al. (2009) studied the effects of copper shock in
marine Synechococcus species indicating that some coastal
water Synechococcus strains may have developed copper
tolerance. While copper may be inhibitory to photosynthe-
sis and other metabolic processes, copper-containing
enzymes greatly influence the net flux of greenhouse gases
to the atmosphere. Two catabolic enzymes have a major
influence on greenhouse gas flux: nitrous oxide reductase,
the terminal step of denitrification, and particulate methane
monooxygenase (pMMO), for removal of methane from the
atmosphere. Dupont et al. (2010) compared metal utiliza-
tion in archaea, bacteria, and eukaryotes through analysis of
protein structures and comparative genomics. Protein
structures for binding of Cu and Zn did not evolve before
the “Great Oxidation Events” of oceans and atmosphere
and resulted in a simultaneous evolution of metal-binding
electron transport proteins involved in redox transforma-
tions of C, N, S, and O necessary for biogeochemical
cycling.
Copper can be introduced into soils via sewage
sludge, mine effluents, agricultural irrigating water, and
industrial waste. Many bacteria have developed a series
of copper-resistance mechanisms to survive the adverse
environment with high level copper concentrations
(Rensing and Grass 2003; Teitzel and Parsek 2003;
Waldron and Robinson 2009). Recently, an increased
number of highly copper-resistant microorganisms have
been isolated which show a remarkable resistance to a
wide range of metal ions while surviving in mineral-rich
environments (Dopson et al. 2003; Golyshina and Timmis
2005; Franke and Rensing 2007). Copper pollution in soil,
water, and the atmosphere has become a global environ-
mental problem because of mining, industrial, and agri-
cultural practices (Nriagu and Pacyna 1988). In order to
lessen the environmental impact caused by copper mining
(Fig. 1), useful environmental biotechnological processes
for mining and remediation are being developed. For
example, copper ion resistance and acidic pH tolerance in
bacteria are features that can be utilized not only to
improve bioleaching but also for bioremediation of
copper-contaminated soils.
Recent developments in copper applications
Copper used in wiring, plumbing, cooling, and roofing
account for most of the demand for copper products
(Edelstein 2011). About 10% of copper consumption
consists of consumer and general products used in
agriculture, animal farming, water distribution systems,
and healthcare settings. In these areas, copper applica-
tions are in most part for the control of microorganisms.
The antimicrobial properties, microbial resistance,
growth benefits, toxicity, and deficiency of copper have
been described extensively in the literature. However, the
recent re-assessment of the benefits of antimicrobial
copper follows a proliferation of multiple antibiotic-
resistant and disinfectant-resistant bacterial strains in the
healthcare environment, copper-tolerant plant pathogens,
and continued contamination of water and food supplies
with human pathogens and subsequent disease outbreaks.
Thus, the many re-discovered uses for copper in the war
against pathogens may have advantages and could very
well result in an increased demand for copper products
and also provide some solutions to the existing chal-
lenges for already environmentally impaired copper
mining sites.
238 Appl Microbiol Biotechnol (2011) 91:237–249