The role of iron-oxidizing bacteria in biocorrosion: a review

Abstract

Lithotrophic iron-oxidizing bacteria depend on reduced iron, Fe(II), as their primary energy source, making them natural candidates for growing in association with steel infrastructure and potentially contributing to microbially influenced corrosion (MIC). This review summarizes recent work on the role of iron-oxidizing bacteria (FeOB) in MIC. By virtue of producing complex 3-dimensional biofilms that result from the accumulation of iron-oxides, FeOB may aid in the colonization of steel surfaces by other microbes involved in MIC. Evidence points to a successional pattern occurring whereby FeOB are early colonizers of mild steel (MS), followed by sulfate-reducing bacteria and other microbes, although studies of aged corrosion products indicate that FeOB do establish a long-term presence. There is evidence that only specific clades of FeOB, with unique adaptations for growing on steel surfaces are part of the MIC community. These are discussed in the context of the larger MIC microbiome.

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The role of iron-oxidizing bacteria in biocorrosion:
a review
David Emerson
To cite this article: David Emerson (2019): The role of iron-oxidizing bacteria in biocorrosion: a
review, Biofouling, DOI: 10.1080/08927014.2018.1526281
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The role of iron-oxidizing bacteria in biocorrosion: a review
David Emerson
Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, USA
ABSTRACT
Lithotrophic iron-oxidizing bacteria depend on reduced iron, Fe(II), as their primary energy
source, making them natural candidates for growing in association with steel infrastructure and
potentially contributing to microbially influenced corrosion (MIC). This review summarizes recent
work on the role of iron-oxidizing bacteria (FeOB) in MIC. By virtue of producing complex
3-dimensional biofilms that result from the accumulation of iron-oxides, FeOB may aid in
the colonization of steel surfaces by other microbes involved in MIC. Evidence points to
a successional pattern occurring whereby FeOB are early colonizers of mild steel (MS), followed
by sulfate-reducing bacteria and other microbes, although studies of aged corrosion products
indicate that FeOB do establish a long-term presence. There is evidence that only specific clades
of FeOB, with unique adaptations for growing on steel surfaces are part of the MIC community.
These are discussed in the context of the larger MIC microbiome.
ARTICLE HISTORY
Received 26 April 2018
Accepted 13 September 2018
KEYWORDS
Iron-oxidizing bacteria;
corrosion;
Zetaproteobacteria;
Gallionellaceae
Introduction
The focus of this review is iron-oxidizing microbes,
with the two specific aims of elucidating the current
state of knowledge about the role they play in micro-
bially influenced corrosion (MIC), as well as under-
standing their role in the context of what is known
about the larger microbiome responsible for MIC.
These microbes oxidize iron as a result of their
metabolism, and many of them can use the electrons
captured from this process as their sole source of
energy for growth. Since steel is composed mostly of
iron, and mild steel (MS) that easily corrodes is the
most common type of steel used in large-scale infra-
structure, there is abundant iron directly available to
support the growth of these organisms. Nevertheless,
the chemical behavior of iron is complex, with bio-
logical and abiological processes both playing a role
in oxidation that varies based on the specific environ-
mental conditions (Melton et al. 2014). As a result,
this can lead to confusion over the specific role of Fe-
oxidizers in the process of MIC. In addition, Fe-oxi-
dizing microbes are less well studied than other
important physiological groups such as sulfate-reduc-
ing bacteria, thus it is not surprising that less is
known about the specific role they may play in MIC.
The last decade has seen increasing interest in the
environmental role of Fe-oxidizing bacteria, and spe-
cifically their role in biocorrosion.
As a whole, corrosion is generally estimated to
account for about 3% of global gross domestic product
(GDP) through the destruction and replacement costs
of steel infrastructure. More precise estimates of costs
specific to MIC compared to corrosion in general are
challenging, nonetheless it is reasonable to say that on a
global basis the costs of MIC run into billions of dollars
annually. There are a number of reviews and mono-
graphs describing the basic processes of MIC that lead
to accelerated corrosion of steel (Beech & Sunner 2004;
Little & Lee 2007; Dang & Lovell 2016). Since the con-
cept of MIC was introduced, certain physiological types
of microbes have been associated with the process.
Principle among these are the sulfate-reducing bacteria
(SRB) whose anaerobic metabolism can produce corro-
sive metabolites and electrochemical conditions that
aggressively promote MIC. Methanogenic archaea are
another group receiving increased attention for their
role in creating cathodic conditions on steel surfaces
that can enhance corrosion (Dinh et al. 2004).
Methanogens and SRB are very distinct from one
another physiologically and genetically, yet given the
right conditions their metabolism predisposes them to
playing a role in MIC. A summary showing both the
potential processes and the complexity of MIC is shown
in Figure 1. There is still much to know about the ecol-
ogy of the MIC process as a whole, as well as specific
metabolic pathways that influence MIC, and the
CONTACT David Emerson demerson@bigelow.org
ß2019 Informa UK Limited, trading as Taylor & Francis Group
BIOFOULING
https://doi.org/10.1080/08927014.2018.1526281

identification of key organisms—especially under nat-
ural settings.
As mentioned above, this review will focus on
those microbes, primarily bacteria, capable of lithoau-
totrophic or chemosynthetic growth on ferrous iron,
Fe(II); however, it is important to consider the other
reactions between microbes and iron as well, since
they can be important, and also the source of some
confusion. Table 1 presents metabolic reactions rele-
vant to iron that are important for biocorrosion.
Lithoautotrophy refers to microbes that gain energy
from the oxidation of ferrous iron to ferric iron
(Fe(III)), and use this energy to fix carbon dioxide
(CO
2
) as the cell’s primary source of carbon.
Heterotrophic Fe-oxidation refers to microbes that
actively catalyze the oxidation of Fe(II), but do not
gain energy from the process, nor do they fix CO
2
,
instead using organic matter as a carbon and energy
source. Exemplars of this process are organisms like
Leptothrix discophora and Sphaerotilus natans that
produce proteins or enzyme systems that actively
catalyze Fe-oxidation, or Mn-oxidation, yet derive no
energetic benefit from it (Ghiorse 1984). It is also
important to remember that at circumneutral pH,
Fe(II) readily oxidizes in the presence of O
2
resulting
in the spontaneous precipitation of Fe-oxyhydroxides
(rust). These oxides can passively adsorb bacteria,
thus the mere association of a bacterium with Fe-oxy-
hydroxides does not prove whether it is catalytically
oxidizing Fe(II), or playing a more passive role (Small
et al. 1999). One potential example of this are
Sediminibacterium spp., a genus within the
Bacteroidetes, a bacterial phylum best known for its
capacity to grow on complex organic matter
(Fern
andez-G
omez et al. 2013). In the corrosion lit-
erature a number of papers refer to
Sediminibacterium as a member of the iron-oxidizing
bacteria (Wang et al. 2012; Li et al. 2014,2015;
Jin et al. 2015) in part due to the finding of 16S
rRNA genes related to this organism being found
in DNA extracted from corrosion products. Yet the
original description of S. salmoneum, isolated from
a eutrophic lake (Qu & Yuan 2008), or subsequent
descriptions of newly isolated Sediminibacterium
Figure 1. Diagram of the processes involved in MIC. This provides an overview of the complex of reactions that can take place
at the metal surface, and in the resultant biofilm. Bioavailable iron would be in the form of Fe
2þ
, substituting of Me
nþ
, shown
in the diagram. X-denote unknown anions. (From Beech et al. 2014.)
2 D. EMERSON

species (Kim et al. 2016), do not make any mention
of the capacity to either oxidize Fe(II), or use it as a
sole electron donor. Additional issues arise when, in
the course of laboratory experiments, cells are grown
with compounds like ferrous citrate, where citrate
may serve as a carbon/energy source, and it can then
be difficult to assess if oxidation of Fe(II) is actually
catalyzed by the bacteria or occurring spontaneously
(Xu et al. 2007; Liu et al. 2017).
An additional source of confusion regarding micro-
bial Fe-oxidation centers around nitrate-dependent
Fe-oxidation. Nitrate-reduction, typically coupled to
the oxidation of organic matter, is a very common
microbial metabolism. The kinetics and thermody-
namics of this reaction coupled to the oxidation of
Fe(II) are favorable for a microbially mediated process
that could support growth, and there is little doubt
that numerous nitrate-reducing bacteria can catalyze
Fe(II)-oxidation (Weber et al. 2006). The problem lies
in showing that these microbes are growing via this
process, i.e. using energy gained from nitrate-depend-
ent Fe-oxidation to fix CO
2
, rather than using organic
matter as their carbon and energy source. The con-
founding factor is that the first step in nitrate reduc-
tion (Table 1) is the production of nitrite (NO
2
) that
can rapidly oxidize Fe(II) chemically (Carlson et al.
2013). As yet, there are no reports of pure cultures of
bacteria that can be readily sustained growing solely
on Fe(II) and nitrate as either obligate, or facultative
nitrate-dependent Fe-oxidizers. There is a well-docu-
mented consortium of microbes, the ‘Straub culture’,
that has been maintained for years and grows via
nitrate-dependent Fe-oxidation, although its potential
to be involved in MIC is unknown (He et al. 2016).
The distinction between anaerobic iron-oxidation
being linked to a product of heterotrophic nitrate
reduction, vs being a lithotrophic process, is import-
ant in terms of determining if a nitrate-dependent
biocorrosion community can sustain itself via lithoau-
totrophy, rather than requiring a significant input of
organic matter.
Another group implicated in anaerobic Fe-oxida-
tion are the photoferrotrophs that are capable of car-
rying out anoxygenic photosynthesis by using Fe(II)
as an electron donor with light (Kappler & Newman
2004). Photoferrotrophy has been documented in sev-
eral groups of photosynthetic microbes, although in
most cases, it is an ancillary, as opposed to a favored,
metabolism for the growth of these cells (Melton
et al. 2014). It is difficult to find well-documented
reports of photoferrotrophs being involved in MIC.
Because these organisms require light, although some
can grow at very low light levels, this limits the pos-
sible MIC habitats to external surfaces where light is
present; however, more research is required to fully
understand the role of photoferrotrophy in MIC.
Lithotrophic, oxygen-dependent Fe-
oxidizing bacteria
Chemolithoautotrophic Fe-oxidizing bacteria (FeOB)
can meet their energy requirements through the oxi-
dation of Fe(II), fix CO
2
and respire with O
2
as an
electron acceptor. They can be broadly classified into
two physiological types, acidophiles and neutrophiles
(Hedrich et al. 2011). Acidophilic FeOB generally
grow at pH 4 or below. At this pH, soluble Fe(II) is
stable in the presence of O
2
, and these bacteria grow
prolifically. However, these environments are rela-
tively rare, especially in terms of places where steel
infrastructure is found, and so will not be considered
further here. FeOB that grow in more circumneutral
conditions, pH 5–8, are common in natural settings
where iron is abundant in sediments and soils
(Kappler et al. 2016). Chemical oxidation of Fe(II)
with O
2
becomes rapid with increasing pH, thus these
organisms prefer anoxic-oxic mixing regions where
O
2
concentrations are low, typically <100 mM, and
Fe(II) concentrations may exceed 10 mM (Rentz et al.
2007). Under such conditions it is common to find
outgrowths of lithotrophic FeOB, where they often
manifest themselves in microbial mats that range
from being barely visible to centimeters or more thick
Table 1. Examples of different types of iron-related metabolisms.
Metabolism Characteristic Reaction
Chemolithoautotroph or chemosynthetic Fe(II) as sole electron donor; CO
2
fixation HCO
3-
þ4Fe
2þ
þO
2
þ8H
2
O!
(CH
2
O) þ4Fe(OH)
3
þ3H
þ
Heterotroph Organic matter as electron donor and C source 4Fe
2þ
þO
2
þ10H
2
O!4Fe(OH)
3
þ8H
þ
Photoferrotroph Either Fe(II) or organics as electron donor; carbon
acquired from either CO
2
or organic carbon
HCO
3-
þ4Fe
2þ
þ10H
2
O!(hv)
4Fe(OH)
3
þ4HCO
3-
þ4H
2
O
2
-dependent/aerobic O
2
as electron acceptor 4Fe
2þ
þO
2
þ10H
2
O!4Fe(OH)
3
þ8H
þ
NO
3
-dependent/anaerobe NO
3
as electron acceptor 4Fe
2þ
þ2NO
3
þ24H
2
O!10Fe(OH)
3
þN
2
þ8H
þ
Direct electron transfer Evidence suggests some anaerobic microbes can
directly take up e
-
without H
2
production
Fe(0) !Fe
2þ
þ2e
-
2H
þ
þ2e
-
!H
2
Note. Direct electron transfer from Fe(0) has yet to be demonstrated in FeOB.
BIOFOULING 3

(Chan et al. 2016). Phylogenetically, the most abun-
dant lithotrophic FeOB in Fe(II)-rich systems delin-
eate themselves quite clearly depending upon whether
they live in marine or freshwater environments. The
former will be considered first.
Marine habitats
In marine systems the most prevalent group of lithotro-
phic FeOB belong to a class of Proteobacteria, the
Zetaproteobacteria, that were first discovered associated
with an Fe(II)-rich hydrothermal vent (Emerson et al.
2007). Thus far all isolates of Zetaproteobacteria are lith-
otrophic Fe-oxidizers. While early discoveries of
Zetaproteobacteria centered around hydrothermal sys-
tems in the deep ocean (where they had previously been
mistaken for freshwater FeOB, see below), more recent
work has expanded their range to essentially any marine
environment, including coastal sediments where Fe(II)
may be in enough abundance to support growth (Scott
et al. 2015;Beametal.2018). As a result, this group may
be thought of as a bio-indicator for an Fe-oxidizing
metabolism. McBeth et al. (2011) published the first
study that demonstrably tied lithotrophic marine FeOB
to the colonization of MS surfaces by showing that MS
coupons incubated in coastal waters in Maine were
colonized by members of the Zetaproteobacteria. Their
presence was detected by microscopic analysis of corro-
sion products, revealing the presence of twisted, helical
stalks coated in iron-oxyhydroxides that are one of the
morphologically unique biosignatures of lithotrophic
FeOB. In addition, using DNA primers specific for the
Zetaproteobacteria, members of this group were identi-
fied as members of the community, and subsequently
representative isolates have been obtained (McBeth et al.
2011; Mumford et al. 2016).
At approximately the same time, the work of Dang
et al (2011) looked at short-term (seven day), in situ
colonization patterns of MS in coastal waters of
China. They found a diverse community of organisms
colonized the steel surfaces, and predominant among
these were members of the Zetaproteobacteria.
Quantitative PCR (qPCR) analysis showed numbers
of Zetaproteobacteria increased by at least four orders
of magnitude during the week long duration of the
incubation, indicating these putative FeOB were
actively growing on the steel surface. A subsequent
successional study of longer duration done on the
coast of Maine showed a similar pattern (McBeth &
Emerson 2016). In this case MS coupons were incu-
bated in both brackish and fully saline coastal sea-
waters for up to 43 days. In both environments a
diverse community was found associated with the
coupon surfaces that, in part, reflected the commun-
ities of nearby sediment, indicating recruitment of
microbial taxa from the sediments. Zetaproteobacteria
were present in both cases and accounted for up to
1–2% of the community. A pattern was seen where
Zetaproteobacteria tended to be earlier colonizers, eg
at 3–13 days, but then either remained static or
declined in numbers at longer time periods (i.e. >2
weeks). Members of the Deltaproteobacteria consist-
ent with recognized taxa of SRBs were present and
showed an increase in numbers with time. In another
parallel to the earlier work of Dang et al. (2011), a
substantial presence of Epsilonbacteraeota, the bacter-
ial phylum formerly classified as the class
Epsilonproteobacteria (Waite et al. 2017), was found
in these incubations. These included relatives of
known sulfur-oxidizing genera like Sulfurimonas
(family Helicobacteraceae) and Arcobacter (family
Campylobacteraceae).
Overall, the results from McBeth and Emerson (2016)
in Maine, and Dang et al (2011) in China, shared similarity
with another study that incubated MS coupons near
Catalina Island (located near Los Angeles, CA) (Barco et al.
2017). Based on analysis of full-length 16S clone libraries,
Barco et al. 2017, found that Zetaproteobacteria abundance
on MS ranged from 0–8% at one month of in situ incuba-
tion, while at two weeks they were not detected. At one
month, Sulfurimonas and Arcobacter represented >50% of
the microbial community, while at two weeks they domi-
nated the community with nearly 90% relative abundance.
Another commonly found taxon was Thiomicrospira,with
abundances ranging from 2% to 4%. In this same study, a
Thiomicrospira strain was shown to grow with Fe(II) as the
sole electron donor. The Deltaproteobacteria including
the family Desulfovibrionaceae were present in one-month
MS samples, suggesting the development of anaerobic
micro-niches.
A more controlled study by Ram
ırez et al. (2016)
examined colonization of either MS or mineral pyrite
surfaces using flow through reactors that were placed
in situ at Catalina Island. These were relatively long
term studies of between two and six months. In this
case, after two months there was visual evidence for
abundant production of stalks by lithotrophic FeOB
on the surfaces of MS. However, molecular analysis
done at six months did not reveal the presence of
Zetaproteobacteria, and morphological analysis found
only remnants of stalk structures indicating the puta-
tive FeOB were not active. Deltaproteobacteria, espe-
cially lineages recognized for sulfate-reduction, were
the most prevalent group identified on MS surfaces,
4 D. EMERSON

with Gammaproteobacteria and Alphaproteobacteria
also being present in appreciable abundance.
Interestingly, the Epsilonbacteraeota were relatively
minor members of the MS community found in this
study, compared to the findings of Dang and McBeth
cited above. It is worth noting that the closed systems
used in these experiments likely encouraged establish-
ment of more strictly anaerobic conditions than might
prevail in a more open system. Overall, consistent
with other studies, this work indicated that stalk-
forming FeOB, presumably members of the
Zetaproteobacteria, were early colonizers of MS, but
as conditions became more reducing, anaerobic com-
munities became prevalent.
Incubation studies are useful for understanding pat-
terns of colonization and succession, but are less
informative about the long-term presence of FeOB in
corrosion products associated with emplaced steel
infrastructure, including shipwrecks. A study of rus-
ticles associated with World War-era II ship wrecks in
the Gulf of Mexico showed evidence for biogenic Fe-
oxides based on scanning electron microscopy. A gene
survey of these rusticles found 16S sequences belonging
to Zetaproteobacteria were present in at least one case,
although the most widespread and prevalent sequences
were associated with putative clades of SRB and sulfur-
oxidizing microbes (Little et al. 2017). Additionally, a
molecular study of World War II-era of corrosion
tubercles in Australia also found the presence of
sequences for M. ferrooxydans, in a complex microbial
community dominated by methanogens (Usher et al.
2014). Another recent study used 16S gene analysis to
compare MS emplaced for eight years at two sites on
the coast of China, along with another set of one-
month-old samples (Li et al. 2017). In this case
Proteobacteria, Firmicutes, and Bacteroidetes were the
dominant phyla, with Proteobacteria accounting for
50–80% of the reads in eight of nine samples. OTUs
belonging to the Deltaproteobacteria dominated the
Proteobacteria, with the majority of these related to
known groups of SRBs, with the genera Desulfovibrio
and Desulfotomaculum having the highest relative
abundances. The Zetaproteobacteria were present in
most of the samples, with relative abundances of
around 0.5–3%. This stands in contrast to the shorter
term colonization studies described above where the
presence of Zetaproteobacteria was found to decrease
over the course of weeks, in some cases to undetectable
levels. A third study, done in France, used a sophisti-
cated reactor system to simulate tidal effects and follow
MS corrosion over nine months under conditions
where the system was either amended or unamended
with organic carbon (Marty et al. 2014). An endpoint
analysis (nine months) found Zetaproteobacteria were
among the more prevalent phylotypes in corrosion
tubercles in the unamended treatments, but were not
found in tubercles associated with the organic treat-
ments. This is consistent with the lithoautotrophic
metabolism of FeOB, where it is unlikely they could
compete with heterotrophs when readily available
organic matter is present. Overall, in the Marty et al
study (2014), SRB were common to all treatments with
the greatest prevalence in the presence of organic
amendment. Together, these investigations of long-
term corrosion products indicate FeOB can become
established as inhabitants of what are presumably quite
stable MIC communities.
While the presence of FeOB in the MIC community
is an important finding, from a practical standpoint,
the capacity for FeOB to accelerate corrosion through
physiological and chemical reactions is also a key aspect
of the process. Lee et al. (2013) studied this using pure
cultures of FeOB, including one isolated from a steel
surface, incubated with MS coupons. The results did
not find evidence for pitting, or a statistically significant
increase in the rate of corrosion over uninoculated con-
trols. Another study that used a reactor system to
understand the dynamics of colonization of steel by
Mariprofundus sp. DIS-1 also did not find evidence for
pitting of steel surfaces, despite rapid colonization
(Mumford et al. 2016). When co-cultures of FeOB and
Fe-reducing bacteria were grown on MS coupons there
was increased surface roughening, although neither
active pitting or a statistically significant increase in
corrosion rate was observed (Lee et al. 2013).
Freshwater habitats
The microbes responsible for lithotrophic Fe-oxida-
tion in freshwater share common physiological and
morphological attributes with marine FeOB, yet they
belong to different phylogenetic lineages and share
surprisingly few genes (Emerson et al. 2013; Kato
et al. 2015). The most well-characterized freshwater
FeOB that grow at circumneutral pH belong to the
Betaproteobacteria, a distinct taxonomic class com-
pared to the Zetaproteobacteria, with many members
belonging to the family Gallionellaceae, or in the fam-
ily Comamonadaceae (Kappler et al. 2016). The
Gallionellaceae in particular tend to be microaero-
philic, obligate Fe-oxidizers, some of which produce
extracellular stalks that are very similar to those pro-
duced by Zetaproteobacteria. The role of FeOB in
steel corrosion in freshwater is less well understood
BIOFOULING 5

or studied than in marine or brackish waters. One
exception to this relates to studies on the corrosion of
steel dock pilings in Duluth-Superior Harbor on Lake
Superior. This harbor has a large amount of emplaced
steel infrastructure due its importance as an ore ship-
ping center, and aggressive corrosion has been
observed (Hicks, 2007). Of particular note are rust
tubercles that form on submerged dock pilings (Little
et al. 2014). Detailed morphological analysis revealed
abundant twisted stalks similar to those produced by
Gallionella ferruginea present inside the tubercles
(Ray et al. 2009). Corresponding with this morpho-
logical evidence for the presence of FeOB, a quantita-
tive molecular analysis found, 16S rRNA gene copies
of the Gallionellaceae accounted for 2–35% of the
total prokaryotic cells present in the corrosion prod-
ucts (Oster, 2012). Interestingly, this same study ana-
lyzed corroding steel in other, smaller harbors on the
north shore of Lake Superior and found little
evidence for FeOB, as well as lower overall rates of
corrosion. This suggests that conditions in Duluth-
Superior Harbor promoted more rapid corrosion and
supported the growth of FeOB. The specific factors
behind this phenomena are yet to be undetermined,
or if there is a direct causal relationship between the
abundance of FeOB and corrosion rate.
It is important to note that MIC in freshwater
systems relates not only to degradation of emplaced
steel infrastructure such as bridges, docks, or ships’
hulls, but also infrastructure that could be used to
store chemical or radioactive wastes underground in
steel containers. To understand this latter process
Rajala et al. (2015) used 100 m deep underground
waste repository tunnels to incubate steel coupons in
slightly brackish and hypoxic groundwater.
Interestingly, the mere presence of the steel coupons
in these oligotrophic groundwaters increased both
the abundance (nearly 100 fold) and diversity of the
groundwater community. Betaproteobacteria were the
most prevalent bacterial group and included enrich-
ment of OTUs related to Rhodoferax ferrireducens
and Sideroxydans spp. Sideroxydans (a member of
the Gallionellaceae) preferentially grows on Fe(II)
under microaerobic conditions, although some strains
can also utilize reduced sulfur-compounds for growth
(Emerson et al. 2013). As the name implies, R. ferrire-
ducens is a known Fe-reducing bacterium; however, it
belongs to the family Comamonadaceae, a group of
microbes with very diverse metabolisms that could
include Fe-oxidizers. Thus it is difficult to confidently
assign a function to OTUs in this group. Sulfate
reducing bacteria were also enriched on the coupons
in this experiment, and were suspected of contribu-
ting to pitting and enhanced corrosion of the
steel surfaces.
The majority of studies in freshwater have focused
on the role of FeOB as agents of clogging and
biofouling in water wells. This process can be coupled
to corrosion as well (Yang et al. 2014; Little et al.
2017); however, it is difficult to distinguish between
the effects of actual biocorrosion, ie the microbially
influenced breakdown of steel infrastructure vs the
occlusion of pipes by the growth and accumulation of
biofilms on the interior surfaces of the pipes. It is
common for the groundwater being pumped through
these systems to have relatively high (tens to hun-
dreds of micromolar) concentrations of Fe(II) that
can support the growth of FeOB, thus the organisms
Figure 2. Example of biofouling in a water-well production pipe where the build-up of Fe-oxides is largely due to the growth of
FeOB. In this case the primary source of Fe(II) is coming from groundwater, not from the steel pipe itself. In addition to physical
clogging, extensive biofilm growth can also lead to corrosion depending upon chemical conditions. (From Wang et al. 2014.)
6 D. EMERSON

may be growing on in situ Fe(II), and not from the
extraction of Fe(II) from iron or steel pipes (Szewzyk
et al. 2011). FeOB are common inhabitants of aquifers
used as water sources for drinking water or other
water supplies (Braun et al. 2016), thus their move-
ment into pipelines and conduits used for transport-
ing water is straightforward. An example of this
comes from a study of dewatering wells from a mine
in Germany where there were high Fe(II) concentra-
tions in the groundwater, and there was nearly com-
plete occlusion of pipelines by microbial biofilms
(Wang et al. 2014). The microbial community con-
tained a high abundance, in some cases close to 50%,
of FeOB related to Gallionella, and stalked morpho-
types were observed in the Fe-oxide rich biofilms.
The authors proposed that Gallionella colonized
the surfaces, and as it grew formed an Fe-oxide rich
biofilm that was continually colonized by other bac-
teria (Figure 2) and ultimately this led to development
of a robust microbial community growing inside
the pipe.
Perspectives on the role of FeOB in MIC
Model for biofilm formation by FeOB
The work discussed above makes a strong case that
lithotrophic FeOB are capable of growing on Fe(II)
released from steel surfaces, and that they are likely
early colonizers and integral members of the MIC
community. Based on these findings, a primary role
for FeOB in MIC may be in the development of eco-
logical associations within the larger microbial com-
munity or microbiome responsible for MIC. These
associations may be more significant to the process
than direct physiological interactions between FeOB
and the metal surface. Thus, it is reasonable to postu-
late that their most important role may be in the early
Figure 3. Schematic of how stalk-forming Zetaproteobacteria may help to initiate growth on steel surfaces in marine habitats.
During the early phase of colonization O
2
penetrates the biofilm, while stalk-forming Fe-oxidizers attach to the surface and grow
outward, taking advantage of the Fe(II) released from the metal surface. Another microbial group often found during this early
phase of colonization is the Epsilonbacteraeota, although their metabolic role is as yet unclear. As the biofilm grows and
ages (lower panel), the number of Zetaproteobacteria decreases, however the stalks remain and continue to accumulate iron
oxyhydroxides forming a denser matrix; O
2
penetration decreases in the biofilm and metabolic groups such as SRB and methano-
gens colonize the biofilm that may lead to more aggressive corrosion. Based on work from Mumford et al. (2016).
BIOFOULING 7

colonization of the steel surfaces coupled with
the production of a 3-dimensional biofilm that can
help initiate more complex biofilm development.
A descriptive model shown in Figure 3 is derived
from detailed studies by Mumford et al. (2016) of the
early phases of colonization of steel by pure cultures
of Zetaproteobacteria. Based on this model, during
the early phase of colonization of steel surfaces
exposed to O
2
, stalk-forming FeOB attach and grow
out from the surface taking advantage of Fe(II) being
released from the steel. As noted above, groups of
Epsilonbacteraeota have also been found in the early
stages of biofilm formation, although their overall
role in the process is not clear. Proteomic analysis of
MS incubated in situ in seawater (Barco et al. 2017)
indicated that hydrogenases of Epsilonbacteraeota,
in particular Sulfurimonas spp., were among the
most abundantly expressed proteins. Whether this is
evidence of H
2
-metabolism linked to lithotrophic
growth on H
2
by these bacteria in corrosive biofilms,
or intracellular hydrogenase activity has yet to be
shown. Lithotrophic growth on H
2
, as well as reduced
S compounds, is consistent with general knowledge of
the metabolism of this phylum (Campbell et al. 2006),
although it cannot be ruled out that they may also
metabolize Fe(II).
As the biofilm on the steel surface expands and
ages, anoxic regions develop, likely due to the con-
sumption of O
2
both by lithotrophic and hetero-
trophic bacteria, with the latter group growing on
organic matter within the biofilm. These regions of
anoxia open niches for anaerobes like SRB and
methanogens to grow and develop a more mature
MIC microbiome that may accelerate the corrosion
process. In this model the abundance of FeOB may
decrease, at least initially, yet the scaffolding of
Fe-oxides they leave behind produces surfaces that
facilitate colonization by other microbes. In ecological
parlance the FeOB play the role of ecological
engineers, where their activity plays a larger role in
ecosystem development than their abundance might
imply (Jones et al. 1994). What is also of interest is
the fate of FeOB in highly aged biocorrosion habitats
where tubercles of rusted steel have formed. As cited
above, there are multiple instances in the marine
environment where Zetaproteobacteria have been
found either in long-term incubations, or in legacy
corrosion products. These findings suggest there may
be a third stage to the model described in Figure 3,
where there is a redevelopment of Zetaproteobacteria
once an MIC microbiome is well established. They
also raise the possibility that at least under some
conditions recycling of Fe(II), perhaps through inter-
actions with the sulfur cycle, could lead to re-release
of Fe(II) to support the growth of FeOB. This is an
area that will require further investigation. In fresh-
water corrosion products, less is known about the
development of MIC communities, or the long-term
presence or fate of FeOB associated with MIC.
However, one study that examined 6–7 year old rust
tubercules on steel dock pilings found evidence for
the presence of freshwater FeOB, indicating they also
can become members of long-term freshwater MIC
communities (Thomas, 2016).
Specific adaptations of Zetaproteobacteria for
growth on steel
To develop a more nuanced understanding of the role
of Zetaproteobacteria in the development of marine
corrosive biofilms it is necessary to have more know-
ledge about which lineages are most associated with
the process. In this regard, it is important to remem-
ber that abundant zero valent iron in steel is a prod-
uct of the Anthropocene, thus microbes have had
relatively little time to adapt to it as a primary growth
substrate. A recent comprehensive phylogenetic ana-
lysis of Zetaproteobacteria found that of 13 relatively
abundant Zeta OTUs (ZOTU) or phylotypes that are
globally distributed, only two of these, ZOTU18 and
ZOTU9, were associated with corrosion (S. McAllister
and C. Chan, pers. comm.). This analysis indicates
there must be some selective pressure for those
ZOTUs that can colonize steel. One possibility is that
they have a greater tolerance for O
2
than is typical for
most Zetaproteobacteria, which grow in low O
2
environments. Steel surfaces exposed to fully oxygen-
ated seawater, as is typical of many environments
with steel infrastructure, may require FeOB to have
a greater capacity to detoxify toxic oxygen products,
or reactive oxygen species, that can result from
reactions of Fe(II) and O
2
(Imlay 2013). This capacity
has been shown for the one cultured representative
of ZOTU18 (Mariprofundus sp. DIS-1), an obligate,
lithotrophic, stalk-producing Fe-oxidizer that has
more detoxification genes for O
2
than any other
isolate of the Zetaproteobacteria (Mumford et al.
2016). Interestingly ZOTU9 also has a cultured repre-
sentative, Ghiorsea bivora, isolated from a hydrother-
mal vent, that can grow on hydrogen as well as Fe(II)
(Mori et al. 2017). While this organism has fewer O
2
detoxification genes than Mariprofundus DIS-1, it is
quite possible that G. bivora can take advantage of H
2
that may be produced as a result of corrosion proc-
esses on steel surfaces, and would act to select this
8 D. EMERSON

specific lineage of Zetaproteobacteria. These examples
suggest how evolutionary adaptations have likely
given these particular lineages an advantage for grow-
ing on steel.
Chemical vs electrochemical induced corrosion
Much of the research on MIC has viewed it as a
chemically mediated process where the production or
consumption of metabolites, for example hydrogen
sulfide or hydrogen, by microbial growth is the key to
accelerating corrosion. This process is referred to as
chemical microbially influenced corrosion (CMIC).
One of the most striking recent discoveries about
MIC is the capacity for anaerobic microbes to channel
electrons directly from the metallic iron surface to the
cell where energetically favorable redox reactions take
place that provide the cell energy for growth. This
process is referred to as electrical microbially influ-
enced corrosion (EMIC). It is most well documented
in SRB, and there is evidence that certain species of
SRB are especially adapted to carry out EMIC, and
that they can cause very aggressive corrosion (Enning
& Garrelfs 2014). There is also evidence for methano-
gens and acetogenic bacteria to stimulate corrosion
through EMIC (Kato et al. 2014; Deutzmann et al.
2015). EMIC is an example of a more wide-ranging
process referred to as extracellular electron transfer
(EET), referring to the uptake or release of electrons
at or outside a microbe’s external cell wall (Lovley
2011; White et al. 2016; Shi et al. 2016). FeOB are an
example of microbes that oxidize Fe(II) at the cell
exterior and transfer the electrons to the electron
transport chain that energizes the cell on the inner
cytoplasmic membrane of the cell (He et al. 2017).
Therefore, it is reasonable to ask if FeOB could bene-
fit from EMIC whereby electrons are directly shuttled
or conducted from the Fe(0) on the steel surface to
the cell itself without the necessity of an intermediate
–Fe(II). So far there is no evidence to directly
support this process in FeOB, especially as a means of
accelerating steel corrosion, as has been shown in
SRB. Presumably to take advantage of EMIC, it would
be most advantageous for FeOB to adhere directly to
the steel surface, thereby minimizing the conductive
path for electrons from substrate to cell. Thus far,
isolates of FeOB that grow well on MS all produce
stalks that attach to the metal surface translocating
the cell away from the surface, which increases the
distance between the cell and the metal surface
(Mumford et al. 2016). These organo-metallic stalks
are composed primarily of ferrihydrite-like iron-
oxyhydroxides, a poorly conductive mineral (Chan
et al. 2010; Toner et al. 2012). One interesting possi-
bility is that in more mature corrosive biofilms where
SRB are present and complex mineral crusts form
that include iron sulfides, FeOB could take advantage
of the conductive properties of these minerals.
Indeed, this mechanism of mineral enhanced con-
ductivity has been proposed as an important means
for sulfate-reducers to carry out EMIC under strictly
anaerobic conditions (Enning et al. 2012). It might be
possible that under micro-oxic conditions there are
FeOB that could capture electrons directly from these
minerals as well, although further research is required
to answer this. Coupled to this is the need to gain
a better mechanistic understanding of how FeOB
conserve energy via Fe-oxidation. Significant progress
has been made on this front recently with the identifi-
cation of a porin-cytochrome c complex protein
(Cyc2) that has been found in all known freshwater
and marine lithotrophic FeOB to date (Barco et al.
2015; Chan et al. 2018). This protein has iron oxidase
activity, and is highly expressed in environments
where biogenic Fe-oxidation is active. As such, Cyc2
has utility as a functional marker for FeOB (Chan
et al. 2018); however many details about biological
Fe-oxidation remain to be elucidated.
Practical implications
Of practical interest is determining whether or not
FeOB play a positive or negative role in accelerating
the process of MIC. Based on the research done to
date, it is too early to fully define their role. Given
the overall complexity of the process of MIC in terms
of both microbial, as well as physico-chemical factors,
it may be the effect of FeOB is more situational,
rather than definitively negative or positive. As
discussed above, initial studies have not shown that
FeOB by themselves rapidly accelerate corrosion,
although when grown in co-culture with Fe-reducers
there is additional roughening of steel surfaces.
Previous work looking at the solitary effects of the
Fe-reducing bacterium Shewanella oneidensis on MIC
showed the process had some inhibitory effect on
corrosion. It was theorized that production of Fe(II)
as a result of reduction of Fe-oxyhydroxides led to
enhanced O
2
consumption near the metal surface
due to the re-oxidation of Fe(II) (Dubiel et al. 2002;
Lee & Newman 2003). However, other studies
indicate H
2
consumption coupled to Fe-reduction by
Fe-reducers can facilitate biocorrosion (Sch€
utz et al.
2015) Further work with co-cultures, or ideally
synthetic consortia of Fe-oxidizers and reducers along
BIOFOULING 9

with sulfate-reducers and perhaps hydrogenotrophs
could help to develop a better understanding of both
synergistic effects of the microbial community on cor-
rosion, as well as improve mechanistic understanding
of the process. Ultimately, the goal for a better under-
standing of how the MIC microbiome functions is to
develop strategies that alter environmental conditions
to select for ecological associations that reduce MIC,
or specific treatments that selectively inhibit the most
aggressive microorganisms responsible for MIC (Kin
& Ballim 2012; Kip & van Veen 2014). Significant
insight into the microbiome responsible for MIC has
been achieved over the last decade (cf Vigneron et al.
2016). Nonetheless, there is still much to understand
about the process. It will be especially important to
better elucidate the dynamics and specific role(s) of
different functional groups in the MIC microbiome,
such as Fe-oxidizing and Fe-reducing microbes, for
the development of effective ecosystem management
practices for treating biocorrosion.
Acknowledgements
The author thanks Dr Joyce McBeth and Dr Adam
Mumford for their efforts on biocorrosion-related studies
done in his laboratory that provided the foundation for
this review. He is also grateful to Dr Roman Barco for
commenting on, and improving an earlier draft of
the manuscript.
Funding
Funding for this study was provided by the US Office of
Naval Research [grant #N00014-08-1-0334].
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