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Nature Reviews Microbiology
nature reviews microbiology https://doi.org/10.1038/s41579-023-00920-3
Review article Check for updates
Microbially mediated
metal corrosion
Dake Xu 1,2, Tingyue Gu 3,4,5,6 & Derek R. Lovley 1,7
Abstract
A wide diversity of microorganisms, typically growing as biolms,
has been implicated in corrosion, a multi-trillion dollar a year problem.
Aerobic microorganisms establish conditions that promote metal
corrosion, but most corrosion has been attributed to anaerobes.
Microbially produced organic acids, sulde and extracellular
hydrogenases can accelerate metallic iron (Fe0) oxidation coupled
to hydrogen (H2) production, as can respiratory anaerobes consuming
H2 as an electron donor. Some bacteria and archaea directly accept
electrons from Fe0 to support anaerobic respiration, often with c-type
cytochromes as the apparent outer-surface electrical contact with the
metal. Functional genetic studies are beginning to dene corrosion
mechanisms more rigorously. Omics studies are revealing which
microorganisms are associated with corrosion, but new strategies for
recovering corrosive microorganisms in culture are required to evaluate
corrosive capabilities and mechanisms. Interdisciplinary studies of the
interactions among microorganisms and between microorganisms
and metals in corrosive biolms show promise for developing new
technologies to detect and prevent corrosion. In this Review, we explore
the role of microorganisms in metal corrosion and discuss potential
ways to mitigate it.
Sections
Introduction
Key reactions in microbial
metal corrosion
Microbial corrosion of metals
under aerobic conditions
Microbial corrosion of metals
under anaerobic conditions
Microbial diversity in metal
corrosion
Mitigating microbial corrosion
Outlook
1Electrobiomaterials Institute, Key Laboratory for Anisotropy and Texture of Materials (Ministry of Education),
Northeastern University, Shenyang, China. 2Shenyang National Laboratory for Materials Science, Northeastern
University, Shenyang, China. 3Department of Chemical & Biomolecular Engineering, Ohio University, Athens,
OH, USA. 4Department of Biological Sciences, Ohio University, Athens, OH, USA. 5Institute for Corrosion and
Multiphase Technology, Ohio University, Athens, OH, USA. 6Institute for Sustainable Energy and the Environment,
Ohio University, Athens, OH, USA. 7Department of Microbiology, University of Massachusetts, Amherst, MA, USA.
e-mail: gu@ohio.edu
Nature Reviews Microbiology
Review article
in the complex biofilms associated with corrosion outside the labora
-
tory. The understanding of microbial corrosion of non-ferrous metals
is even more poorly understood. The goal of this Review is to critically
review the previous research on microbial metal corrosion and its
prevention and to highlight exciting opportunities for future research.
Key reactions in microbial metal corrosion
In the air, Fe0 is abiotically oxidized with the reduction of oxygen (O2)
(Fig.2a, reaction 1), and the Fe
2+
generated is further abiotically oxi-
dized to Fe(III) oxides, generating the familiar ‘rust’ associated with
corroding iron. Aqueous environments foster the growth of chemically
and physically heterogeneous biofilms on metal surfaces populated
with diverse microorganisms. O
2
is often unavailable as an Fe
0
oxidant
within these biofilms. Potential Fe0 oxidants under anaerobic condi-
tions include protons (H
+
), nitrate, Fe(III), sulfate, carbon dioxide (CO
2
)
and hydrogen sulfide (H
2
S). Only H
+
(Fig.2a, reaction 2) and H
2
S (Fig.2a,
reaction 3) react abiotically with Fe
0
, generating H
2
(refs. 9,12–14). Fe
0
oxidation with other potential electron acceptors requires micro-
bial catalysis (Fig.2a, right), in which a diversity of microorganisms
(Table 1 and Fig.2b) accept electrons from Fe
0
to support anaerobic
respiration, either directly or indirectly via mechanisms detailed later.
Fe
2+
generated from these various reactions can react with sulfide,
carbonate, phosphate or additional iron ions to produce a wide range
of minerals (Fig.2a, reactions 4–9), which typically accumulate on
corroding iron, becoming incorporated in biofilms, and are visual
signs of intense corrosion. Key to understanding the factors control-
ling the rate and extent of iron corrosion in specific environments
is discerning which of these many possible reactions is taking place
within corrosive biofilms.
Similar to Fe0, metallic nickel (Ni0), metallicaluminium (Al0),
metalliczinc (Zn
0
) and metallictitanium (Ti
0
) readily react with O
2
,
generating metal oxides of the metals that can form a protective film,
reducing additional O
2
access to the underlying metal and trapping
metal ions resulting from the metal oxidation at the surface, making
further metal oxidation thermodynamically unfavourable (Fig.2c).
However, if the passive film becomes damaged, exposing the under-
lying metals to water under anaerobic conditions, the metals will
reduce H
+
to H
2
(refs. 15,16). By contrast, the oxidation of metallic
copper (Cu0) is too electropositive to directly generate H2 (ref. 17),
but in sulfidogenic environments H
2
S can react with Cu
0
to release H
2
(refs. 17,18) (Fig.2d).
Microbial corrosion of metals under aerobic
conditions
Biofilms of Fe2+-oxidizing bacteria along with the Fe(III) oxides that
are generated from the Fe
2+
oxidation (Fig.2a) are commonly associ-
ated with corrosion of ferrous metals. In aqueous environments, Fe2+-
oxidizing bacteria accelerate the oxidation of Fe
2+
to ferric ion (Fe
3+
)
coupled to O
2
reduction over the abiotic reaction rate
19
. These include
lithoautotrophic bacteria such as Mariprofundus, Gallionella and Sider-
oxydans spp., which conserve energy from Fe2+ oxidation that is then
used to fix CO2, and heterotrophs such as Leptothrix and Sphaerotilus
spp., which grow heterotrophically and catalyse Fe2+ oxidation without
energetic benefit19. Rapid removal of Fe2+ should promote abiotic Fe0
oxidation coupled to O2 reduction (Fig.2a, reaction 1) by reducing
Fe
2+
accumulation. In low pH environments, such as those inhabited
by Acidithiobacillus ferrooxidans, soluble Fe3+, which has a high redox
potential, is also an Fe0 oxidant (Fig.2a, reaction 9), generating more
Fe
2+
to further support A. ferrooxidans respiration
20
. Thus, corrosion of
Introduction
Of the many important impacts of microbial biofilms, corrosion is the
most economically damaging, accounting for more than two-thirds of
all expenses attributed to biofilm growth and activity
1
. The more than
US$2.7trillion annual cost of microbial corrosion dwarfs the biofilm
costs associated with human health, food and agriculture, and energy
and the environment combined
1
. Well-known examples of the cata-
strophic impact of microbial corrosion include the notorious 2006
Alaskan pipeline leak, which in addition to environmental damage
disrupted global oil markets2. In the United States alone, water leaks
associated with corrosion of water distribution pipes, much of it attrib-
uted to microbial activity, will require a trillion-dollar investment in
new infrastructure over the next 25years
3
. Microbial corrosion impacts
not only pipelines but also a diversity of other structures and devices
including nuclear waste storage facilities, heat exchangers, reinforced
concrete, oil and gas infrastructure, water utilities, fuel systems, power
plants, underground storage tanks, marine platforms, offshore wind
turbines and dental devices (Fig.1).
Humans have been producing metallic iron (Fe
0
) for only a few
thousand years. Thus, corrosion processes associated with micro-
organisms probably evolved for reasons other than utilizing Fe0 as an
energy source. For example, the microbial hydrogen (H2) oxidation that
is key to some forms of microbial corrosion is a likely reflection of the
early evolution of H2 metabolism and the continued importance of H2
as a central intermediate in many modern anaerobic environments
4
.
Microorganisms that can corrode by directly extracting electrons
from metals are likely to use mechanisms previously evolved for micro-
bial electron extracellular exchange with minerals and other microbial
species5,6.
Few microbiologists have studied microbial corrosion, despite
its economic and environmental impacts. The study of microbial cor-
rosion shares many core concepts and analytical methods with other
microbiology subdisciplines (Box1), and corrosion investigations
seem to be entering a renaissance era in which new, interdisciplinary
approaches are beginning to provide fresh insights into the ways in
which microbial activity can cause metal corrosion. Better understand-
ing of corrosion mechanisms is expected to lead to improved strategies
for detecting corrosion before it causes severe damage, and to new
approaches for corrosion mitigation.
Microorganisms can deteriorate the quality of many metals includ-
ing aluminium, copper, nickel and titanium, but most microbiological
research has focused on the role of microorganisms in the corrosion
of iron-containing ferrous metals, such as carbon and stainless steels
7
.
Corroding iron metals are typically covered with biofilms (Fig.1) of
diverse structure and function that initially promote deterioration
of the metal by oxidizing Fe0 to ferrous ion (Fe2+):
Fe →Fe+2e (1)
02+−
For this reaction to proceed, the electrons (e–) released from Fe0
must be transferred to one of a diversity of potential electron-accepting
molecules (Fig.2a).The question that has been asked for more than a
century8 is which of the myriad possible abiotic and microbiological
reactions involving Fe
0
(Fig.2a) are the most important. The popularity
of different mechanisms has waxed and waned over time and there is
still little consensus on how microbial corrosion takes place. Detailed
histories of microbial corrosion research are available elsewhere
9–11
.
Only a few proposed mechanisms have been rigorously evaluated under
well-defined laboratory conditions and none have been demonstrated
Nature Reviews Microbiology
Review article
iron-containing steel was threefold to sixfold faster in the presence of
A. ferrooxidans than in sterile controls, even when A. ferrooxidans was
not in direct contact with the iron20.
At circumneutral pH, Fe2+-oxidizing isolates have shown mixed
results for whether pure cultures accelerate iron corrosion19,21–24. Fe3+
combines with hydroxyl ions to form Fe(III) oxides (Fig.2a, reaction 4),
a
Microbial corrosion
Various industries
Power plants Fuel systems Water utilities Oil and gas Rebar and
concrete
Heat
exchangers
Nuclear waste
storage
Oshore
assets
Ships and
port facilities
Dental
devices
Manned
spacecraft
Marine environments Medical Space
Other
Alcaligenes
Zoogloea
Diaphorobacter
Azospirillum
Uncultured
Anaerospora
Paludibacter
Desulfovibrio
Desulfomicrobium
Petrimonas
Opitutus
Erysipelothrix
Brevundimonas
Xanthobacter
Sporomusa
Magnetospirillum
Pseudomonas
Hydrogenophaga
Relative abundance of bacteria (%)
10
20
30
40
50
60
70
80
90
100
0
Halomonas
Methanosphaerula
Methanoregula
Nitrosopumilus
Unclassiied
Mathanobacterium
Methanomassiliicoccus
Methanolinea
Aquisphaera
Desulfitibacter
Methanospirillum
Methanosphaera
Methanothermobacter
Methanomethylovorans
Nitrososphaera
Methanoculleus
Methanothrix
Methanosarcina
Relative abundance of archaea (%)
10
20
30
40
50
60
70
80
90
100
0
100.00 µm
50.00 µm
194.30 µm
150.00 µm
0.00 µm
Width: 636.4 µm Height: 636.4 µm Depth: 194.3 µm
30 µm 0
50
100
y (µm)
z (µm)
x (µm)
Largest pit
depth = 26 µm
150
200
250
300
300
34
0
050 100 150 200 250
25 µm
20 µm
15 µm
10 µm
5 µm
0 µm
b
e f
c d
Fig. 1 | Examples of microbial corrosion. a, Diversity of materials that are
susceptible to microbial corrosion. Areas affected by corrosion include various
industries, such as oil and gas, water utilities and power plants, as well as marine
environments, and space and medical sectors. b, Severe microbial corrosion of a
carbon steel pipeline used in shale gas production. c, Biofilm associated with the
corroding carbon steel surface imaged with confocal scanning laser microscopy.
d, Confocal scanning laser microscopy image of carbon steel, after removal of
biofilm and corrosion products, revealing the morphology of pits generated
by microbial corrosion. e,f, Heatmaps of the diversity of bacteria (part e) and
archaea (part f) on the surface of a corroding carbon steel pipeline. Parts b,c
and d unpublished data from Dake Xu laboratory. Parts e and f replotted with
data from ref. 87.
Nature Reviews Microbiology
Review article
which precipitate on cells and the metal surface
19,23
. Depending on con-
ditions, Fe(III) oxides may or may not abiotically oxidize Fe0 (ref. 25).
Mn(IV) oxides produced by Mn2+-oxidizing bacteria are strong Fe0
oxidants. Fe0 oxidation with Mn(IV) regenerates Mn2+ (refs. 25–27).
The Mn
2+
-mediated electron shuttling between Fe
0
and Mn
2+
-oxidizing
bacteria corrodes Fe
0
faster than direct abiotic Fe
0
oxidation with O
2
(Fig.3a). In a similar manner, elemental iodine (I
2
) oxidizes Fe
0
, pro-
ducing the iodine ion (I–). Then, I−-oxidizing bacteria regenerate I2 to
further promote Fe0 oxidation28. In this way, corrosion is microbially
accelerated in pipelines carrying water with high concentrations of I2
(ref. 28).
Fe2+-oxidizing and Mn2+-oxidizing bacteria are early biofilm
colonizers, consuming O
2
, generating oxide coatings on the metal
surface and creating a low O2 environment near the biofilm–
metal interface
19,22,27
. Heterotrophic microorganisms contribute to
O2 removal within corrosion biofilms because organics are avail-
able to microorganisms in many environments in which corrosion
eventually develops29. As O2 is depleted deeper within biofilms,
microorganisms capable of fermentative metabolism and anaerobic
respiration become established near the metal–biofilm interface19,30,
where anaerobic microbial activity promotes corrosion via multiple
mechanisms (Fig.3a).
Box 1
The interconnection of corrosion biolms research with other
disciplines
The study of microbial corrosion can advance other microbiology
subdisciplines, which share common concepts and experimental
approaches, and vice versa. Electrotrophy, the direct uptake
of electrons from extracellular electron donors, is a rapidly
evolving ield not only in corrosion but also in microbial ecology,
bioengineering and biogeochemistry6. For example, the question
of the relative role of direct metal-to-microorganism electron transfer
or hydrogen (H2)-mediated electron transfer in metal corrosion
parallels inquiries into the relative importance of direct interspecies
electron transfer and interspecies H2 transfer feeding methanogens
in anaerobic digesters, soils and sediments130. Identiication of
microorganisms capable of serving as the electron-accepting partner
for direct interspecies electron transfer is revealing microorganisms
that are also eective in corrosion via direct metal-to-microorganism
electron transfer35. Challenging questions key for optimizing
microbial electrosynthesis — the bioelectrochemical production
of organic commodities from carbon dioxide (CO2)131–134 — are
similar to those for corrosion: do microorganisms primarily accept
electrons from electrodes via H2, electron shuttles or direct
electrode-to-microorganism electron transfer; and which electron
transfer method is most practical for scaling. Corroding metal
surfaces, which select for microorganisms that are highly eective
in extracting electrons from electroactive surfaces, might be an
excellent environment for recruiting microorganisms well adapted
for electron uptake from cathodes in electrosynthesis. Elucidation
of mechanisms for electron uptake from cathodes yields insights into
how microorganisms might accept electrons from Fe0 (refs. 62,135).
The study of bioelectrochemical technologies and microbial
corrosion already relies on similar electrochemical techniques to
document the rate, extent and type of electron exchange (Box2).
Adhesion to metal and bioilm development is a key feature of
corrosion136. Thus, advancements in bioilm theory90,137,138 have clear
application to corrosion. In turn, future investigation of corrosion
bioilm development, composition and diversity has the potential
to contribute general knowledge to bioilm ecology and evolution
in complex environments.
Fig. 2 | Key reactions and diversity of microorganisms involved in metal
corrosion. a, Key reactions associated with microbial corrosion of ferrous
metals. Each of these reactions has been shown to be thermodynamically
favourable under conditions related to corrosion. Numbers 1–9 refer to abiotic
reactions associated with corrosion. b, Diversity and spatial heterogeneity
of microorganisms within a biofilm involved in corrosion of ferrous metals.
Hydrogen (H2)released from metallic iron (Fe0)and produced by fermentative
bacteria (representative genera in grey box, left) is consumed by denitrifiers
(green box), sulfate reducers (yellow box), methanogens (light blue box) and
acetogens (red box). Heterotrophs (magenta box), sulfide-oxidizing consortia
(yellow box) and iron oxidizers (grey box, right) consume O2 promoting
anaerobic corrosion reactions. Electroactive methanogens (magenta box) and
Fe(III) reducers (orange boxes) directly extract electrons from Fe0 generating
ferrous ion (Fe2+)that iron oxidizers convert to Fe(III) oxides that serve as an
additional electron acceptor for Fe(III) reducers. The diffusion of organics
and electron acceptors (oxygen (O2), nitrate (NO3–), sulfate (SO42–)) from the
surrounding environment into the biofilm and their preferential consumption
with the biofilm (O2, then NO3–, then SO42–), as well as the availability of Fe0 as
an electron donor at the base of the biofilm, results in vertical heterogeneity
of diverse functional populations. Lightning bolts designate direct electron
transfer from Fe0 to cells. c, Key reactions associated with the corrosion of
aluminium, zinc and titanium. Films of metal oxides, hydroxides and/or sulfides
block O2 and proton (H+)contact with the underlying metal and the outward
diffusion of metal ions. Microbial or chemical damage to the films permits O2
and H+ to access the metal and allows the release of metal ions generated from
the metal oxidation. d, Key reactions associated with copper corrosion. Under
aerobic conditions, metallic copper (Cu0)is abiotically oxidized and the cupric
ion (Cu2+)generated combines with microbially produced oxalic acid, forming
insoluble copper oxalate precipitates. Under anaerobic conditions, sulfate
reducers produce hydrogen sulfide (H2S) that reacts with Cu0 to generate H2
and copper sulfide (Cu2S) precipitates. Al0, metallic aluminium; CH4, methane;
CH3COOH, acetic acid; CO2, carbon dioxide; CO32–, carbonate; e–, electron;
Fe3+, ferric ion; FeCO3, ferrous carbonate; Fe3O4, magnetite; Fe(OH)3, iron
hydroxide; FePO4, ferric phosphate; FeS, iron sulfide; H2O, water; N2, nitrogen;
NH4+, ammonium; OH, hydroxide; PO43–, phosphate; S2–, sulfide; SO42–, sulfate;
Ti0, metallic titanium; Zn0, metallic zinc.
Nature Reviews Microbiology
Review article
O2H2O
O2
Iron oxidizers
H2O
OH–
Fe(OH)3FeS
5–8
Fe2+
Fe0Fe2+
Fe
2+
Fe
0
Fe2+
S2–
CO3
2–
PO4
3–
Fe3+ H+
Fe
2+
Fe
0
Fe
2+
Fe
0
H2
Respiratory
anaerobes
H2
Fe3+
CH4, acetate
S2–
Fe2+
N2, NH4
+
Succinate
CO2
SO4
2–
Fe(III)
NO3
–
Fumarate
Ferrous minerals:
sulide, carbonate,
phosphate, magnetite
Electrons transferred to microorganisms
via numerous mechanisms (Fig. 3)
Fe0
H2S + Fe0
e–
Al3+, Zn2+, Tin–
Outward diusion
blocked inhibiting
further metal oxidation
Microbially or chemically
damaged passive ilm
Undamaged passive
ilm of metal oxides,
hydroxides, sulides
O2, H+ penetration
blocked
Al0
Zn0
Ti0
Al3+
Zn2+
Tin+
e–
1 2 Fe0 + 4 H+ + O2
2 Fe0 + 2 H+
3 Fe0 + H2S
4 Fe3+ + 3 OH–
5 Fe2+ + S2–
2 Fe2+ + 2 H2O
Fe2+ + H2
FeS + H2
Fe(OH)3
FeS
6 Fe2+ + CO3
2–
7 3 Fe2+ + 2 PO4
3–
8 Fe2+ + 2 Fe3+ + 8 OH–
9 Fe0 + 2 Fe3+
FeCO3
Fe3(PO4)2
Fe3O4 + 4 H2O
3 Fe2+
Abiotic reactions
CO2 + 8 H+ + 8 e–
2 CO2 + 8 H+ + 8 e–
SO4
2– + 8 H+ + 8 e–
Fe(III) + e–
2 NO3
– + 12 H+ + 10 e–
NO3
– + 10 H+ + 8 e–
Fumarate + 2 H+ + 2 e–
CH4 + 2 H2O
CH3COOH + 2 H2O
S= + 4 H2O
Fe2+
N2 + 6 H2O
NH4
+ + 3 H2O
Succinate
Anaerobic respiration
4 Fe2+ + 4 H+ + O24 Fe3+ + 2 H2O
Aerobic respiration
H2H+
H2O
H2O
H2O
Fe(III)
Fe(III)
Fe(III)
Fe0
Fe2+
H2H+
Fe0Fe2+
Fe0Fe2+
Fe
2+
Fe
0
Fe0
Al0, Zn0 or Ti0
Acetobacterium
Sporomusa
Methanobacterium
Methanococcus
Methanosarcina
Methanosaeta
NO3
–
Fe2+
NH4
+
Fe2+
Fe2+
Acetate CO
2
H2
H2
H+
CO
2
O
2
O
2
CO
2
CO
2
O
2
H2H+
CO
2
CH
4
CH
4
SO
4
2–
SO
4
2–
SO
4
2–
S
2–
S
2–
H2H+
H
2
H
+
NO3
–
NO3
–
O2
N2
H2
Organics
Organic acids
Clostridia
Bacillus
Enterobacter
Anaerolinea
Mariprofundus
Dechloromonas
Sideroxydans
Pseudomonas
Marinobacter
Thalassospira
Desulfovibrio
Desulfoferrobacter
Desulfotignum
Desulfobacula
Desulfobulbus
Sulfur-oxidizing
consortia
Precipitation
Vibrio
Pseudoalteromonas
Flexibacter
Marinobacter
Fe2+
Geobacter
Shewanella
Geobacter
Geothrix
Rhodoferax
Organic acids
Organics
Biofilm
a
b
c
O2, H+H2OH2S H2
Microbially produced oxalic acid Microbially
produced sulide
Microbial
consumption
Copper oxalate
precipitate
Cu0
Aerobic Anaerobic
d
Cu0Cu2+
Cu2+
C C
O
O
O–
O–Cu2S precipitate
Cu0
12
4
93
Organics
Microbial consumption
O2H2OH2H+
Nature Reviews Microbiology
Review article
The role of aerobic bacteria in the corrosion of non-ferrous metals
does not seem to have been intensively investigated, but microorgan-
isms can accelerate corrosion under aerobic conditions, presumably
by releasing metabolites that destroy the protective metal oxide films
occluding the underlying metal31,32. The fungus Aspergillus niger pro-
duced organic acids, lowering the pH to promote the oxidation of
Cu0 (Fig.2d). Oxalic acid, the most abundant acid produced, further
accelerated corrosion by chelating the cupric ion (Cu2+) generated from
Cu0 oxidation and forming copper oxalate precipitates33.
Microbial corrosion of metals under anaerobic
conditions
Unlike O2, potential oxidants for Fe0 in anoxic environments, such
as nitrate, sulfate and CO2, do not spontaneously abiotically react
with Fe0 to oxidize and corrode it. Microbial catalysis is required.
Hence, microorganisms have their greatest impact on corrosion of
ferrous metals in anaerobic environments. The activity of anaerobic
microorganisms promotes the oxidation of Fe
0
through multiple mech-
anisms (Fig.3b,c) including the production of metabolites that enhance
the oxidation of Fe
0
to Fe
2+
with the reduction of H
+
to H
2
; H
2
-mediated
electron transfer between the metal and the microorganism; direct
metal-to-microorganism electron transfer; and redox-active organic
molecules shuttling electrons between Fe0 and microorganisms. These
corrosion mechanisms have been associated with phylogenetically
and physiologically diverse microorganisms (Table1 and Figs.1,2).
In some instances, corrosion mechanisms are considered rigor-
ously defined, with genetic studies or other approaches that defini-
tively rule out alternatives. In other studies, the mechanisms have only
been inferred from indirect evidence (Table1). Until recently, micro-
organisms and iron sources were typically added to poorly defined,
Table 1 | Examples of the diversity of microorganisms participating in Fe0 oxidation under anaerobic conditions and
proposed corrosion mechanisms
Microorganism Relevant physiology and
electron acceptor Fe0 as sole
donor Fe0 forms Proposed mechanism
Acetobacterium spp. Acetogen; CO2+13,124 Pure Fe0 (refs. 13,124) H2 intermediate (V)13,124
Archaeoglobus Hyperthermophile, acetogen;
CO2 heterotroph; SO42– +125; –125,126 Carbon steela,125; carbon steel126 Sulide (I)125; direct (I) but H2
utilizer125,126
Bacillus licheniformis Fermentative dissimilatory nitrate
reduction –Carbon steela,97; X80 steelb,98;
stainless steelc,72 Direct (I)97,98; ribolavin (I)72
Clostridium celerecrescens Fermentative –API XL 52 steeldOrganic acids54
Desulfoferrobacter sulitae H2-oxidizing sulfate reducer +Pure Fe0H2 intermediate and direct (I)127
Desulfopila corrodens (strain IS4) H2-oxidizing and lactate-oxidizing
sulfate reducer +Pure Fe0 (refs. 36,61); mild
steele,51 H2 intermediate (I); direct (I)51,61
Desulfovibrio ferrophilus (strain IS5) H2-oxidizing and lactate-oxidizing
sulfate reducer +Pure Fe0 (refs. 36,61); mild steel51 H2 intermediate (I)36; direct (I)51,61
Desulfovibrio vulgaris H2-oxidizing and lactate-oxidizing
sulfate reducer +13,38; –60 Pure Fe0 (refs. 13,38); carbon
steel60; carbon steel17 H2 intermediate(V)13,38; direct (I)60;
lavin shuttle (I)17
Dethiosulfovibrio peptidovorans Fermentative, thiosulfate reducer –Mild steel Unspeciied128
Enterobacter roggenkampii Fermentative –Carbon steel Organic acids44
Geobacter spp. Electroactive with fumarate,
nitrate and Fe(III) as electron
acceptors
+14,34,36 Pure Fe0 (ref. 14); stainless
steel34,36 Direct (V)14,34
Methanospirillum hungateiMethanogen +13 Pure Fe0 (ref. 13) H2 intermediate (V)13
Methanobacterium spp. Methanogen +12; +71 Pure Fe0 (ref. 12); carbon steel71 H2 intermediate (V)12; H2
intermediate and direct (I)71
Methanococcus spp. Methanogen +12 Pure Fe0 (refs. 12,59) H2 intermediate (V)12,57,59,95
Methanosarcina barkeri Methanogen +Carbon steel Electron shuttle (I)96
Methanosarcina acetivorans Methanogen +Fe0; stainless steel Direct (V)35
Prolixibactersp. Nitrate reducer –Fe0Direct (I)70 or H2 (I)7
Pseudomonas aeruginosa Nitrate reducer –Carbon steel Electron shuttle (I)99
Shewanella oneidensis Electroactive, fumarate, nitrate +37; –29 Carbon steel37; stainless steel29 H2 intermediate (V)37; direct (V)29,37
Sporomusa spp. Acetogen +Fe0H2 intermediate (I)124,129
Sulfurimonas sp. Sulide-oxidizing nitrate reducer –Carbon steel Nitrite and sulfur intermediates100
Wolinella succinogenes Nitrate reducer +13 Pure Fe0 (ref. 13) H2 intermediate (V)13
CO2, carbon dioxide; Fe0, metallic iron; H2, hydrogen; I, mechanism inferred from indirect evidence; SO42–, sulfate; V, mechanism veriied. aCarbon steels composed of approximately 99% Fe0
combined with small amounts of carbon, manganese, phosphate, sulfur and sometimes silica. bX80 steel composition: 0.093wt% carbon, 0.069wt% silicon, 1.85wt% manganese, 0.013wt%
phosphate, 0.0068wt% sulfur, 0.3wt% chromium, 0.15wt% nickel, 0.19wt% copper, 0.038wt% aluminium, 0.011wt% titanium and balance Fe0. c316L stainless steel: 0.019wt% carbon, 0.43wt%
silicon, 1.18wt% manganese, 0.032wt% phosphate, 0.0006wt% sulfur, 10.5wt% nickel, 16.78wt% chromium, 2.09wt% molybdenum and balance Fe0. dAPI XL 52 steel: 0.11wt% carbon, 0.955wt%
manganese, 0.175wt% silicon; 0.005wt% phosphate, 0.022wt% sulfur, 0.037wt% chromium, 0.293wt% copper, 0.013wt% nickel and balance Fe0. eMild steel >99.37% iron.
Nature Reviews Microbiology
Review article
organic-rich media for mechanistic studies7,9. Elucidating the routes
for corrosion in such systems is difficult because multiple types of
microbial metabolism can take place simultaneously. Understanding
corrosion dynamics under complex conditions such as those found
in real-world situations is the ultimate goal. However, studies with Fe0
as the only electron donor available to support respiration, coupled
with quantitative monitoring of respiration and appropriate controls
to account for the possible role of electron shuttles, can yield more
readily interpretable results
7,9,14,34–37
. Functional genetic studies
14,34,35,37,38
or other approaches that can associate a loss of protein function with
an inhibition of corrosion in model corrosion isolates, or possibly even
within mixed-species corrosion communities
39
, are among the most
powerful tools to reveal corrosion mechanisms. In the future, compara
-
tive molecular analysis of zones of high and low corrosion rates
40–49
may reveal important microorganisms, corrosion mechanisms and
diagnostic molecular signals for corrosion without the need to first
culture isolates. With further study, other parameters, such as isotope
fractionation or type of mineral formation, might be developed into
diagnoses for different mechanisms of iron corrosion21,50,51.
H2 as an intermediary electron carrier
Electron transfer between Fe0 and microorganisms via a H2 intermediary
has been central to discussions of microbial Fe0 corrosion, as this was
first proposed as the mechanism by which sulfate reducers promote
corrosion52. Even at circumneutral pH, the protons available in water can
abiotically accept electrons from Fe
0
to generate H
2
(refs. 12–14) (Fig.2a,
reaction 2). Lower pH supplies more H
+
, favouring H
2
production. Thus,
the release of CO2, acetic acid (CH3COOH) and other short-chain fatty
acids during microbial metabolism accelerates corrosion
53,54
. Micro-
bial oxidation of the H
2
at the metal surface recycles H
+
, avoiding net
H+ consumption during Fe0 oxidation and making H+ available at the
surface for additional Fe0 oxidation. Localized zones of lower pH, and
thus higher corrosion, may form within heterogeneous biofilms, lead-
ing to pitting of the metal
53,55
. Hydrogenases released from cell lysis
56–58
,
or that are actively secreted outside the cell
59
, catalyse H
2
production.
H2S produced during microbial sulfate reduction may also react with
Fe
0
to enhance H
2
production, either through a direct reaction with Fe
0
(Fig.2a, reaction 3) or iron sulfide (FeS) deposits providing a conductive
surface to facilitate electron transfer from Fe0 to H+ (ref. 25).
Anaerobes aggressively compete for H2 in anaerobic environ-
ments4. Thus, rapid microbial H2 uptake is likely to maintain low H2
concentrations during corrosion, thermodynamically favouring fur-
ther reduction of H
+
to H
2
(ref. 13). When microorganisms capable of
H
2
utilization are deprived of organic electron donors
60
, more aggres-
sive corrosion may be a metabolic adaption to gain more energy from
Fe0 oxidation via H2. Diverse microorganisms reducing either nitrate,
fumarate, Fe(III), sulfate or CO2 have all been shown to anaerobically
oxidize H
2
produced from Fe
0
(Table1). Faster corrosion of Al
0
and
Zn0 in the presence of H2-utilizing sulfate-reducing bacteria suggests
that microbial H2 uptake also promotes corrosion of these metals15,16.
Several different experimental strategies have been used to dem-
onstrate the importance of H2 as the electron carrier between Fe0 and
microorganisms. Early studies physically separated Fe
0
and micro-
organisms, permitting only gas exchange12,13. In an elegant study, the
effectiveness of Methanococcus maripaludis strains in Fe
0
corrosion
was linked to the presence of genes for an extracellular hydrogenase
59
.
Studies with a mutant of Desulfovibrio vulgaris unable to use H2 dem-
onstrated that a H2 intermediary electron carrier was essential for
Fe0 to serve as an electron donor for sulfate reduction38. By contrast,
deleting the uptake hydrogenases of Shewanella oneidensis only partly
prevented corrosion, demonstrating that H
2
uptake was just one of the
routes for Fe0 oxidation37.
Methods for genetic manipulation are not yet available for many
corrosive microorganisms. An alternative approach to evaluate
whether microorganisms rely on H
2
as an electron carrier between Fe
0
and cells is to determine their ability to use 316L-grade stainless steel,
which does not generate H2, as an electron donor34,36. For example, it
was proposed that the sulfate reducers Desulfovibrio ferrophilus and
Desulfopila corrodens were capable of direct metal-to-microorganism
electron transfer because they oxidized Fe
0
much faster than other
H
2
-utilizing isolates
61
. However, such comparisons are not a defini-
tive criterion for direct electron transfer, as evidenced from the
M. maripaludis extracellular hydrogenase studies59 described above,
in which the strains that corroded Fe0 the fastest employed an extra-
cellular hydrogenase. D. ferrophilus and D. corrodens could use pure
Fe0 as an electron donor, but not 316L stainless steel, suggesting that
they relied on H2 as an electron carrier to oxidize Fe0 (ref. 36). Digest-
ing outer-surface proteins with protease did not inhibit D. ferrophilus
sulfate reduction with Fe
0
as the electron donor
62
, also suggesting
dependence on an electron carrier, such as H2, that is oxidized within
the cell. The mechanisms of Fe
0
corrosion by D. ferrophilus are of great
interest because its rate of corrosion above abiotic controls (1.6mm
per year uniform corrosion; 1.5cm per year pitting corrosion, which is
a localized form of corrosion where cavities are formed in the material)
exceeds severe corrosion rates in pipelines
63,64
. Therefore, now that
methods for making gene deletions in D. ferrophilus are available
65
, the
role of H2 as an intermediary electron carrier for D. ferrophilus corrosion
should be further evaluated with hydrogenase gene deletion studies
similar to those recently demonstrated for D. vulgaris38.
Direct metal-to-microorganism electron transfer
Direct metal-to-microorganism electron transfer, known more simply
as electrobiocorrosion, refers to corrosion when the initial electron
acceptor for electrons derived from Fe
0
is an outer-surface electrical
contact on the cell surface. Electrobiocorrosion has been observed for
several microorganisms in which the possibility for H2 uptake could
be rigorously ruled out14,29,34,36,37. In each of these studies, an outer-
surface, multi-haem c-type cytochrome was implicated as an important
electrical contact between Fe0 and the corroding microorganism. For
example, a strain of Geobacter sulfurreducens genetically modified
to prevent H
2
uptake, as well as wild-type Geobacter metallireducens,
which cannot use H2, reduced either fumarate, nitrate or Fe(III) oxide,
with pure Fe0 or stainless steel as the electron donor14,34,36. Deletion of
genes for outer-surface, multi-haem c-type cytochromes known to
be involved in other forms of extracellular electron exchange inhib-
ited electron uptake from Fe0 in both Geobacter strains. Fe0 served as
the electron donor for the reduction of CO
2
to methane by Methano-
sarcina acetivorans, which is unable to use H2 as an electron donor35.
Deletion of the gene for MmcA, a multi-haem membrane-bound c-type
cytochrome, previously shown to be involved in electron transport to
extracellular electron donors
66
and electron uptake from other cells
67
,
inhibited methane production with Fe0 as the electron donor35. All of
the cells of the Geobacter and Methanosarcina spp. seemed to be in
direct contact with the metal
14,34,67
, suggesting that potential strategies
for long-range electron transport over multiple cell lengths, such as
electrically conductive pili
5
, were probably not necessary for corro-
sion. However, the ability of some electroactive microorganisms68 and
mixed microbial communities
69
to form conductive biofilms suggests
Nature Reviews Microbiology
Review article
that, under some circumstances, microorganisms at a distance from
the metal surface could contribute to direct electron uptake from iron.
Simultaneous electron uptake via a H
2
intermediate and outer-
surface c-type cytochromes is possible
37
. Deletion of the genes for
one or more of the outer-membrane multi-haem c-type cytochrome
conduits responsible for other forms of extracellular electron exchange
in S. oneidensis partially inhibited Fe
0
oxidation
29,37
, but, as noted above,
so did deletion of uptake hydrogenases37.
Several other claims for direct metal-to-microorganism elec-
tron transfer have not been rigorously evaluated. For example,
direct electron uptake was proposed for a nitrate-reducing Prolixi-
bacter sp.
70
, but the apparent consumption of H
2
during Fe
0
corro-
sion suggests that H2 served as an intermediary electron carrier7.
Similar concerns exist for claims that Methanobacterium strains
IM1 (ref. 61) and TO1 (ref. 71) are capable of direct electron uptake
because they can utilize H2, and the possibility that their high corrosion
Initial colonization by Fe2+
oxidizers and heterotrophs
Mechanism 1:
Producing an O2-consuming bioilm to
provide a habitat for corrosive anaerobes
Mechanism 2:
Microbial recycling of Fe0 oxidants
Passivation layer of Fe(III) oxide blocks
key microbial corrosion mechanisms
Corrosion enabled
Sulfate reducer
Respiration depletes
O2 in bioilm
Corrosive anaerobes grow
in anaerobic zones
Fe2+ oxidizer
Fe0
Fe0
I2
Fe
2+
Fe
0
I–
Fe3+
Mn4+ Mn2+
Fe2+
Fe2+, Mn2+ or I– oxidizer
O
2
H
2
O
Anaerobe
Outer surface cytochromes
Potentially corrosive
microorganisms
Conductive minerals
X
reduced
X
oxidized
Fe
2+
Fe
0
Fe
2+
Fe
2+
Fe
2+
Fe
0
X
reduced
X
oxidized
Fe
0
Fe
0
Fe
2+
Fe
0
Fe0
H
+
, CO
2
2H
+
2H
+
H
2
H
+
H
2
, organics
Fe
2+
Fe
0
Fe
2+
Fe
0
Fe
2+
X
reduced
X
oxidized
Flavin
oxidized
Flavin
reduced
Fe
0
Fe0
Sulide
minerals
facilitate H2
production
Organic acids
neutralized and
diusion restricted
Restricted diusion
of H+ in and H2 out
limiting H2 production
Fe(III) reducers
remove Fe(III) oxide
CH3COOH
CH3COOH
CH3COO–
Hydrogenase
catalyses H2
production
SO
4
2–
S
2–
X
reduced
X
oxidized
Lower pH favours
Fe0 oxidation
Organic acids–COOH
Fermentable substrate Xreduced = CH4, S2–, N2, Fe(II), succinateXoxidized = CO2, SO4
2–, NO3
–, Fe(III), fumarate
Organic acids–COO–
Fe
2+
X
reduced
X
oxidized
Fe
0
2H
+
H
2
Fe(III) oxide layer
Insulating Fe(III) oxide
blocks electron transfer
to potentially corrosive
microorganisms
Direct electron transfer to
corrosive microorganisms
H
+
H
2
H
+
H
+
H
2
H
2
H
2
Fe
2+
Fe
0
Fe
2+
Fe
0
H
+
Fe
2+
Fe
0
CO
2
CH
4
SO
4
2–
S
2–
Heterotroph
a
b
c
d
Nature Reviews Microbiology
Review article
rates are due to the release of hydrogenases or other factors cannot
be discarded.
Organic molecules as electron carriers between metals and
microorganisms
Redox-active organic molecules are possible alternatives to H2 as
intermediary electron carriers between Fe
0
and anaerobic respira-
tory microorganisms during corrosion (Fig.3c). Organic electron
shuttles important in other forms of extracellular electron exchange,
such as mineral reduction and interspecies electron exchange, include
humic substances and a diversity of microbial metabolites, such as
flavins, phenazines and pyocyanins5. Faster corrosion in cultures of
sulfate-reducing D. vulgaris or D. ferrophilus was attributed to ribofla-
vin functioning as an electron shuttle
63,72–74
. However, it has yet to be
demonstrated that Fe0 reduces riboflavin, or that reduced riboflavin
can serve as the electron donor for sulfate reduction, the two reactions
necessary for riboflavin to function as a shuttle. Riboflavin amend-
ments did not stimulate sulfate reduction in cultures of D. vulgaris with
Fe
0
as the sole electron donor
38
and the midpoint potential of flavins
seems to be too positive for flavins to function as an electron shuttle
for microbial reduction of sulfate to sulfide
25,38
. Flavins play multiple
roles in microbial physiology, with functioning as extracellular elec-
tron shuttles being one of the least common. Strategies designed to
specifically detect electron shuttling, such as separating the corrod-
ing metal and the microorganisms by incorporating the metal within
microporous beads
75
or genetic modifications that prevent extracel-
lular flavin release76, are potential approaches to further evaluate the
role of organic electron shuttles in Fe0 corrosion.
Pseudomonas aeruginosa accelerated Ti0 corrosion via a mecha-
nism that involved secretion of phenazine-1-carboxylate77. One possi-
bility is that the phenazine is an electron shuttle, accepting electrons
from Ti0, with reduced phenazine serving as an electron donor for O2
respiration. However, key reactions in this model, such as Ti0 reduction
of phenazine and respiration with reduced phenazine as the electron
donor, have yet to be verified.
Another less well-studied impact of anaerobes on corrosion is the
removal or partial damage of protective surfaces known as passivation
layers. For example, the accumulation of Fe(III) oxides, produced either
by Fe2+-oxidizing bacteria or abiotic oxidation (Fig.2a), may obstruct
corrosive microorganisms from attacking the metal. Microbial Fe(III)
reduction can remove the protective layer (Fig.3d), accelerating cor-
rosion
10,78–81
. Extracellular production of hydrogen peroxide associ-
ated with P. aeruginosa release of reduced phenazine oxidized Cr(III)
oxide — an important component of the passivation layer on stainless
steel — to Cr6+, making the stainless steel more vulnerable to corrosion82.
Acidic metabolites may also attack minerals in passivation layers
83
.
Passive film damage is particularly important for very active metals
such as Ti0, Al0 and Zn0, because they readily react with water without
a passive film.
Microbial diversity in metal corrosion
In addition to the diversity of microorganisms shown to enhance
corrosion of metals in pure culture (Table1), molecular analyses of
microbial communities associated with corroding metal surfaces have
described a wide diversity of bacteria and archaea enriched within
corrosion biofilms
30,41–45,47,49,84–90
. Physiological diversity (Table1 and
Fig.2b) determined from studies with defined cultures includes aerobes
(heterotrophs, iron-oxidizing and sulfur-oxidizing bacteria), facul-
tative microorganisms (heterotrophs, nitrate reducers) and diverse
anaerobes including fermenters, dissimilatory nitrate reducers, Fe(III)
and Mn(IV) reducers, sulfate reducers, methanogens and acetogens.
In molecular studies of mixed communities, phylogenetic characteri-
zation, which has often been at the level of family or above, provides
insufficient physiological information to infer a substantial role in
corrosion because corrosion rates can vary substantially even between
species of the same genus
63
. Furthermore, some microorganisms within
corrosion biofilms may not significantly contribute to corrosion but
simply utilize the metal surface as a support for growth on nutrients
in the surrounding environment and/or nutrients released from the
microorganisms actively engaged in corrosion43,47,48,86,90,91.
Although progress is being made towards identifying genes that
could indicate a high potential for microbial corrosion within a micro-
bial community46, it is not yet possible to predict corrosion mechanisms
from the presence of specific genes. For example, although gene dele-
tion studies have indicated that in some microorganisms outer-surface,
multi-haem cytochromes are important electrical contacts for direct
electron uptake from Fe
0
(refs.
14,34,35,37
), the presence of similar genes in
other microorganisms may not be indicative of a direct electron uptake
capability
36
. Many microorganisms that are capable of exchanging
electrons with other microbial species, minerals or electrodes lack
outer-surface c-type cytochromes5, and might also electrically interact
with metals during corrosion. The presence of hydrogenase genes is
not necessarily predictive of the ability of microorganisms to use H2 as
an intermediary electron carrier for corrosion35.
Therefore, it is still necessary to study representative isolates to
determine whether microorganisms within corrosion biofilms are likely
to have the possibility to enhance corrosion and to evaluate their cor-
rosive mechanism(s). Corrosion is often associated with a high abun-
dance and metabolic activity of sulfate reducers
41,45,48,91–93
, most notably
Desulfovibrio spp., which have served as model microorganisms for
Fig. 3 | Details of key mechanisms for microbial corrosion of ferrous metals.
a, Under aerobic conditions, iron-oxidizing microorganisms colonize the
metal surface and develop biofilms that provide zones of low oxygen (O2)that
enable the growth of corrosive anaerobes, such as sulfate reducers. In another
mechanism, iron-oxidizing, manganese-oxidizing and iodine-oxidizing
microorganisms generate oxidants for abiotic metallic iron (Fe0)oxidation.
b, Under anaerobic conditions, sulfide minerals formed as the result of microbial
sulfate reduction, and protons released from organic acid fermentation products
promote the oxidation of Fe0 coupled with the reduction of proton (H+)to
hydrogen (H2), as do extracellular hydrogenases released from microorganisms.
c, Anaerobic respiration with Fe0 as the electron donor can occur with
direct metal-to-microorganism electron transfer facilitated by multi-haem
outer-surface c-type cytochromesorconductive minerals. Alternatively, soluble
redox-active molecules, such as flavin, function as an electron shuttle between
Fe0 and the microorganism. Lightning bolts designate direct electron transfer
from Fe0 to cells. d, Fe(III) oxides protect Fe0 from corrosion because they are an
insulating layer preventing direct electron transfer from Fe0 to microorganisms
and restricting access of organic acids and other sources of H+, thus limiting H+
availability for Fe0 oxidation coupled to H+ reduction to H2. When Fe(III) reducers
remove Fe(III) oxides, Fe0 oxidation coupled either to direct electron transfer
or H+ reduction is possible. H2 oxidizers, such as sulfate reducers, oxidize H2,
resupplying H+ for additional Fe0 oxidation. CH4, methane; CH3COOH, acetic
acid; CO2, carbon dioxide; Fe2+, ferrous ion; Fe3+, ferric ion; I–, iodine ion;
I2, elemental iodine; NO3–, nitrate; S2–, sulfide; SO42–, sulfate.
Nature Reviews Microbiology
Review article
corrosion studies since the earliest investigations on microbial cor-
rosion10,11,52. More than 50 corrosion studies have focused on just one
species, D. vulgaris
11
, which as noted above relies on H
2
as an inter-
mediary electron carrier for Fe0 oxidation38. For all sulfate reducers
there is the possibility that production of H2S may directly lead to a
non-enzymatic corrosive reaction of sulfide with Fe
0
, especially at low
pH10 (Fig.2a, reaction 3).
Methanogens can also have an important role in corro-
sion12,13,30,35,46,50,57,59,61,71,94–96. Many methanogens grow with the H2
released from Fe0 as the sole electron donor, as can the corrosive ace-
togens studied to date (Table1). Direct electron uptake has only been
rigorously demonstrated for M. acetivorans35.
As noted above, the Fe(III)-reducing microorganisms G. sulfurredu-
cens, G. metallireducens and S. oneidensis are capable of direct electron
uptake from Fe0 (refs. 14,29,34,37), but both S. oneidensis37 and G. sul-
furreducens14 can also accept electrons from Fe0 via H2. G. metalliredu-
cens and S. oneidensis also directly accept electrons from Fe
0
with nitrate
as the electron acceptor. Amongst other corrosive nitrate reducers,
Wolinella succinogenes grows with H
2
evolved from Fe
0
(ref. 13) whereas
it has been inferred that Bacillus licheniformis72,97,98 and P. aeruginosa99
may take up electrons via direct metal-to-microorganism electron
transfer or an organic electron shuttle (Table1). Nitrite generated from
nitrate reduction may also act as an abiotic oxidant for Fe0 (ref. 100).
Corrosion has primarily been studied with isolates recovered
under culture conditions in which the ability to interact with metals
was not a selective pressure. A better understanding of the diversity of
microorganisms contributing to corrosion will require a rethinking
of isolation strategies to isolate microorganisms representative of
those that predominate in corrosive biofilms7,9. Due to the complex
-
ity of microbial communities involved in corrosion, it seems unlikely
that any one isolate will be able to replicate the full range of corrosive
reactions likely to take place in mature, highly corrosive biofilms
21,86,101
.
Therefore, in order to approximate the microbial corrosive activity in
the real world with laboratory studies it will be necessary to mimic the
diverse communities with biofilms built from appropriate combina-
tions of diverse physiological microbial types
21,22,84,102–104
. For example,
the combination of an Fe(II)-oxidizing isolate with an Fe(III) reducer21
or a sulfate reducer
22
accelerated corrosion beyond that achieved with
individual isolates. Iron was corroded faster when an Fe(III)-reducing
strain of Geobacillus was added to a consortium of two fermentative
Bacillus spp. and the sulfate reducer Desulfotomaculum sp. SRB-M
79
.
In a study involving two species of sulfate reducers, a syntroph and
a methanogen, different combinations of co-cultures and culture
conditions demonstrated the importance of both sulfide and acetate
production in promoting corrosion102.
Mitigating microbial corrosion
Strategies for mitigating microbial corrosion typically rely on physical
and chemical methods for removing biofilms, but biological-based
techniques are evolving (Fig.4). Periodic scrapping to remove biofilms
Ag+
HO
HO
OH
OH
N N
OO
O
O
Pipeline pig Biocide cocktail
Flow
Physical scrubbing (pigging)
with biocide
Cu
Cu
Ag
Ag
Ce Ce
Cu2+
Ce3+
aNovel metal alloy
b
Live cell Dead cell Polymer coating
Biologically produced chemicals
Chelator Surfactant
Metal
Dispersing
Nature-mimicking
peptide
Quorum-sensing
inhibitor
Phage
Replication
D-Amino acid
Coatings
cAntibioilm agents
d
Bioilm dispersal
ePhage therapy
fBifunctional corrosion inhibitor
gProtective bioilm
h
Smart coating
Antimicrobial
Metal
Agent to heal
coating damage
HO
H2N
OH
O
Live cell
Dead cell Antimicrobial
molecule
Corrosion barrier
EPS
Corrosive
microbe barrier
Biomineralization layer
O2 barrier
O2 corrosion
Cell lysis
Fig. 4 | Various methods for disrupting biofilms to prevent or mitigate
microbial metal corrosion. a, Surface scrubbing of a biofilm using a pipeline
pig tool (pigging) coupled with biocide application. b, Novel metal alloys that
incorporate silver(Ag), copper (Cu)and cerium(Ce) release metal ions that
are toxic to corroding microorganisms. c, Plain polymer coating or smart
coating with self-healing ability to repair damage to the coating and release
antimicrobials, thus protecting the metal from corrosion. d, Antibiofilm agents
that inhibit biofilm growth, such as EDTA or surfactant molecules, weaken
microbial activity in biofilms or eliminate biofilms. e, Diverse chemical agents
can disperse biofilms. f, Phage treatment to lyse biofilm cells. g, Bifunctional
corrosion inhibitor molecules can both protect the metal surface and have
antimicrobial activity. h, Protective biofilm can keep corrosive microorganisms
and abiotic corrosive agents, such as oxygen (O2), away from the metal surface.
Cu2+, cupric ion; EPS, exopolymeric substances. Nature-mimicking peptide in
part e adapted with permissionfrom ref. 108, Elsevier.
Nature Reviews Microbiology
Review article
as well as periodic chemical treatments that broadly kill the micro
-
organisms within biofilms is the most common approach105. To limit
corrosion, iron can be alloyed with other metals that either slowly
release biocidal metal ions, such as copper, or with chromium, which
forms a protective oxide layer on the iron surface
7
. Various coatings
that are toxic to microorganisms and/or prevent attachment have
also been developed
7
. However, biological concepts that may be more
environmentally friendly and cost-effective are emerging.
For example, biologically produced chemicals such as -limonene,
a component of citrus peels, may be effective antimicrobials106.
-Amino acids
107
or peptides
108
that either kill microorganisms or serve
as a signal for biofilm dispersal can enhance the effectiveness of tradi
-
tional biocides7,109. Deploying microorganisms that can produce killing
or dispersal agents offers the possibility of continuous in situ genera-
tion of biofilm inhibitors at low cost110. Predatory Bdellovibrio111 or quo-
rum sensing inhibitors112 reduced steel corrosion by sulfate reducers
in laboratory incubations. However, these approaches, or applying
‘cocktails’ of bacteriophages to lyse corrosive bacterial biofilms
109
,
remain aspirational corrosion mitigation goals.
Encouraging the growth of self-sustaining biofilms that can block
corrosive agents is an attractive concept also in need of further devel-
opment
7
. In aerobic environments, biofilms that cover metal surfaces
with an O2-consuming layer limit O2 access to the metal, thus prevent-
ing abiotic oxidation
109
. Reduced minerals formed within biofilms can
also contribute to O
2
removal. Extracellular polymeric substances
can block O
2
, metabolites or microorganisms from accessing metal
surfaces113. Microbially produced carbonate minerals can protect
metal surfaces114. Natural communities contributing to carbonate
formation likely protected the iron sheet piles that reinforce waterways
and dykes in the Netherlands from corrosion over a 50-year deploy-
ment115,116. A highly diverse microbial community, enriched in organic
acid-oxidizing bacteria and methanogens, was enriched near the piles
and was associated with the accumulation of carbonates. An improved
understanding of the mechanisms by which microbial communities in
soils and sediments can promote carbonate precipitation near metal
surfaces could lead to important new strategies for sustainable and
inexpensive corrosion prevention.
An effective field-scale manipulation of the microbial commu-
nity to diminish corrosion is the addition of nitrate, which effectively
promotes the growth of nitrate reducers and inhibits the growth and
activity of more corrosive sulfate reducers
117
. Other microbially based
mitigation strategies that have been based on laboratory studies, typi-
cally with a limited diversity of potentially corrosive microorganisms,
will require much more extensive testing and development before
they will be field applicable7,109.
Outlook
Research to date has conclusively demonstrated that microbial corro-
sion is a serious economic problem that threatens industry, health and
the environment. However, the process is still so poorly understood
that there are inadequate strategies to definitively detect and sustain-
ably mitigate this damaging activity. Improved understanding of which
microorganisms are responsible for corrosion and how they corrode
is essential. Molecular analysis of corrosion communities40–49 will be
an important approach, but more detailed mechanistic studies are
required before it will be possible to meaningfully develop a ‘molecu-
lar or sequence-based Koch’s postulates’118,119 approach to diagnose
microbial corrosion and monitor the success of mitigation strategies.
Needed are attempts to apply Koch’s original culture-based postu-
lates to microbial corrosion with skilful isolation of microorganisms
from corroding materials and evaluation of their corrosive capabili-
ties
7,9
. Comparative genomics and transcriptomics of strains that are
closely related phylogenetically and metabolically, but differ greatly
in their corrosion capabilities, is expected to be a productive avenue
for elucidating corrosion mechanisms.
The development of genetic methods to rigorously evaluate possi-
ble corrosion mechanisms in novel microorganisms will also be needed.
Beyond providing new diagnostic molecular tools for corrosion,
Box 2
Diagnosis and monitoring of microbial corrosion
Diagnosing and preventing microbial corrosion requires methods
not only to estimate the rate and extent of corrosion but, ideally, also
to discriminate between abiotic corrosion and corrosion in which
microorganisms are the causative agents, because the mitigation
of each type of corrosion may be dierent. At present, there is
insuicient information to predict corrosion rates or mechanisms,
or even to deinitely ascertain whether corrosion is taking place,
based on an assay of any microbial genes or proteins7,25. In laboratory
studies, rates of corrosion are commonly determined from
measurements of metal weight loss and assessments of metal pitting
with confocal, atomic force or scanning electron microscopy29,34,37.
A diversity of electrochemical techniques in which the corroding
metal of interest serves as the working electrode are available
and can provide online monitoring with near real-time estimates
of microbial corrosion rates without disrupting bioilm activity7,139.
Scanning electrochemical microscopy is an exciting technology for
simultaneous high-resolution topographical and chemical species
mapping within liquid environments140. Fine-scale electrochemical
variations on the surface of corroding metal can be mapped,
associating microbial cells with microbially catalysed redox reactions
within heterogeneous environments141. Microsensors can potentially
elucidate the availability of electron acceptors and nutrients, as
well as pH and metabolites, at a ine scale within corrosion bioilms
to provide better insights into environmental factors inluencing
microbial activity and reactions at the metal–bioilm interface7,139.
X-ray photo-electron spectroscopy, X-ray diraction and Fourier-
transform infrared spectroscopy can aid in identifying passive ilms
and the mineral products of corrosion7, potentially linking speciic
minerals with mechanisms of corrosion. However, most of the
corrosion monitoring approaches described here are not translatable
to monitoring of corrosion in open, dynamic environments, outside
the laboratory. We need new tools for continuous or periodic
monitoring of microbial abundance, community composition and
activity in order to track microbial corrosion in real time.
Nature Reviews Microbiology
Review article
mechanistic studies will likely yield insights into novel mitigation
approaches. For example, if direct electron uptake from Fe0 via multi-
haem c-type cytochromes and/or H2-mediated metal-to-microorganism
electron uptake are found to be the most important mechanisms for
corrosion, then a search for treatments that specifically target the
cytochromes and hydrogenases will be warranted.
As physiological properties and contributions of individual
components of corrosion biofilms are better understood, there will
be a need to develop an understanding of the web of interactions
between individual populations within biofilms. Most microbial cor-
rosion studies have been conducted with static incubations, over short
times, often in the presence of high concentrations of readily degraded
organic substrates. More realistic conditions of flow, longer times
and organic concentrations and types are likely to yield results more
relevant to actual corrosion environments. Methods are also needed
to specifically evaluate the activity of the ‘bottom feeders’ that are
localized at the metal–biofilm interface and likely to be most active in
corrosion processes even though they may not be the most numerous
microorganisms within the biofilm.
An eventual goal is to build genome-scale metabolic models that
describe the activity of microorganisms in corrosion biofilms and their
interactions with other biofilm components
93
, analogous to similar
applications in host microbiomes, bioremediation, wastewater treat-
ment and biogeochemical cycling120–123. Advances in electrochemical
and imaging methods (Box2) will make crucial contributions to this
complex, interdisciplinary problem25.
There are great opportunities for basic research in microbial metal
corrosion that not only can aid in solving this economically important
problem but also can expand insights into biofilm ecology beyond
those already being developed primarily from the study of medically
relevant biofilms. Thus, the investigation of metal corrosion is highly
recommended to upcoming generations of microbial ecologists,
physiologists and environmental engineers.
Published online: xx xx xxxx
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Acknowledgements
D.X. was inancially supported by the National Key Research and Development Program
of China (No. 2022YFB3808800) and the National Natural Science Foundation of China
(No. U2006219) while working on this Review. The authors apologize to all investigators
whose excellent work could not be cited due to space constraints.
Author contributions
The authors contributed equally to all aspects of the article.
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Reviews Microbiology thanks Daniel John Blackwood,
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