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



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
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.
Received 26 April 2018
Accepted 13 September 2018
Iron-oxidizing bacteria;
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
ß2019 Informa UK Limited, trading as Taylor & Francis Group
identification of key organismsespecially 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
) as the cells 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
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
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
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
, substituting of Me
, shown
in the diagram. X-denote unknown anions. (From Beech et al. 2014.)
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
, 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
) 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
and respire with O
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
, 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 58, are common in natural settings
where iron is abundant in sediments and soils
(Kappler et al. 2016). Chemical oxidation of Fe(II)
with O
becomes rapid with increasing pH, thus these
organisms prefer anoxic-oxic mixing regions where
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
fixation HCO
O) þ4Fe(OH)
Heterotroph Organic matter as electron donor and C source 4Fe
Photoferrotroph Either Fe(II) or organics as electron donor; carbon
acquired from either CO
or organic carbon
-dependent/aerobic O
as electron acceptor 4Fe
-dependent/anaerobe NO
as electron acceptor 4Fe
Direct electron transfer Evidence suggests some anaerobic microbes can
directly take up e
without H
Fe(0) !Fe
Note. Direct electron transfer from Fe(0) has yet to be demonstrated in FeOB.
(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
12% of the community. A pattern was seen where
Zetaproteobacteria tended to be earlier colonizers, eg
at 313 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
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 08% 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
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,
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
5080% 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 0.53%. 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
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 235% 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.)
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
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
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).
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
, 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
-metabolism linked to lithotrophic
growth on H
by these bacteria in corrosive biofilms,
or intracellular hydrogenase activity has yet to be
shown. Lithotrophic growth on H
, 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
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 67 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
than is typical for
most Zetaproteobacteria, which grow in low O
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
(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
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
detoxification genes than Mariprofundus DIS-1, it is
quite possible that G. bivora can take advantage of H
that may be produced as a result of corrosion proc-
esses on steel surfaces, and would act to select this
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 microbes 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
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
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
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.
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 for this study was provided by the US Office of
Naval Research [grant #N00014-08-1-0334].
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... At circumneutral pH, Fe 2+ -oxidizing isolates have shown mixed results for whether pure cultures accelerate iron corrosion 19,[21][22][23][24] . Fe 3+ combines with hydroxyl ions to form Fe(III) oxides (Fig. 2a, reaction 4) (Fig. 3a). ...
... Fe 2+ -oxidizing and Mn 2+ -oxidizing bacteria are early biofilm colonizers, consuming O 2 , generating oxide coatings on the metal surface and creating a low O 2 environment near the biofilmmetal interface 19,22,27 . Heterotrophic microorganisms contribute to O 2 removal within corrosion biofilms because organics are available to microorganisms in many environments in which corrosion eventually develops 29 . ...
... Heterotrophic microorganisms contribute to O 2 removal within corrosion biofilms because organics are available to microorganisms in many environments in which corrosion eventually develops 29 . As O 2 is depleted deeper within biofilms, microorganisms capable of fermentative metabolism and anaerobic respiration become established near the metal-biofilm interface 19,30 , where anaerobic microbial activity promotes corrosion via multiple mechanisms (Fig. 3a). ...
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A wide diversity of microorganisms, typically growing as biofilms, 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, sulfide 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 define 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 biofilms 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.
... Mariprofundus is widespread in the marine environment and capable of autotrophic iron oxidation on steel surfaces, in sediments, and in the water column (Chiu et al. 2017;McAllister et al. 2019). Within steel biofilms, iron-oxidizing bacteria such as Mariprofundus have been implicated as early colonizers, and can use iron released from the steel surface as an electron donor for growth (McBeth and Emerson 2016;Emerson 2018). Through production of extracellular stalks, iron oxidizers may create a specialized niche for successional colonization of steel by microorganisms involved in microbiologically influenced corrosion (Mumford et al. 2016;Emerson 2018). ...
... Within steel biofilms, iron-oxidizing bacteria such as Mariprofundus have been implicated as early colonizers, and can use iron released from the steel surface as an electron donor for growth (McBeth and Emerson 2016;Emerson 2018). Through production of extracellular stalks, iron oxidizers may create a specialized niche for successional colonization of steel by microorganisms involved in microbiologically influenced corrosion (Mumford et al. 2016;Emerson 2018). Sulfurimonas are globally distributed and are chemolithoautotrophic bacteria capable of sulfur oxidation in a variety of marine habitats (Han and Perner 2015;Wang et al. 2021). ...
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The rapidly expanding built environment in the northern Gulf of Mexico includes thousands of human built structures (e.g. platforms, shipwrecks) on the seabed. Primary-colonizing microbial biofilms transform structures into artificial reefs capable of supporting biodiversity, yet little is known about formation and recruitment of biofilms. Short-term seafloor experiments containing steel surfaces were placed near six structures, including historic shipwrecks and modern decommissioned energy platforms. Biofilms were analyzed for changes in phylogenetic composition, richness, and diversity relative to proximity to the structures. The biofilm core microbiome was primarily composed of iron-oxidizing Mariprofundus, sulfur-oxidizing Sulfurimonas, and biofilmforming Rhodobacteraceae. Alpha diversity and richness significantly declined as a function of distance from structures. This study explores how built structures influence marine biofilms and contributes knowledge on how anthropogenic activity impacts microbiomes on the seabed.
... Therein, the sharp and uneven morphology features are more likely to capturing microbes from pipe water due to larger specific surface area (Zhuang et al., 2019). Typically, captured microorganisms would induce other fine mineral deposits filling up the HOS intervals with microbes gradually enveloped into the scale interior (Emerson, 2018). The outer-surface morphology of actual pipe scale is rough and uneven, which is advantageous for the interception of planktonic microorganisms (Fig. 3b, c). ...
... Additionally, the process may significantly alter the dominant genus in biofilms grown on pipe walls, necessitating additional studies. (Wikieł et al., 2014), (Enning et al., 2012), (Ali et al., 2020), (Lan et al., 2022), (Venzlaff et al., 2013), (Anandkumar et al., 2009), (Yang et al., 2014a), (Thyssen et al., 2015), (Lee et al., 2013), (McBeth et al., 2011), (Rao et al., 2000), (Linhardt, 2010), (Emerson, 2018), , (Yang et al., 2014b), (Zhu et al., 2014), (Zhu et al., 2020), Iron reducers/Siderophore-producing bacteria Pseudomonas, Shewanella, Geobacter, Acidobacterium, Anaeromyxobacter, Geothrix, Rhodobacter, Ferribacterium, Microbacterium, Mesorhizobium, Mycobaterium, Rhizobium, Rhodococcus, Nocardia ...
Microbially-induced corrosion (MIC) is unstoppable and extensively spread throughout drinking water distribution systems (DWDSs) as the cause of pipe leakage and deteriorating water quality. For maintaining drinking water safety and reducing capital inputs in pipe usage, the possible consequences from MIC in DWDSs is still a research hotspot. Although most studies have investigated the effects of changing environmental factors on MIC corrosion, the occurrence of MIC in DWDSs has not been discussed sufficiently. This review aims to fill this gap by proposing that the formation of deposits with microbial capture may be a source of MIC in newly constructed DWDSs. The microbes early attaching to the rough pipe surface, followed by chemically and microbially-induced mineral deposits which confers resistance to disinfectants is ascribed as the first step of MIC occurrence. MIC is then activated in the newly-built, viable, and accessible microenvironment while producing extracellular polymers. With longer pipe service, oligotrophic microbes slowly grow, and metal pipe materials gradually dissolve synchronously with electron release to microbes, resulting in pipe-wall damage. Different corrosive microorganisms using pipe material as a reaction substrate would directly or indirectly cause different types of corrosion. Correspondingly, the formation of scale layers may reflect the distribution of microbial species and possibly biogenic products. It is therefore assumed that the porous and loose layer is an ideal microbial-survival environment, capable of providing diverse and sufficient ecological niches. The usage and chelation of metabolic activities and metabolites, such as acetic, oxalic, citric and glutaric acids, may lead to the formation of a porous scale layer. Therefore, the microbial interactions within the pipe scale reinforce the stability of microbial communities and accelerate MIC. Finally, a schematic model of the MIC process is presented to interpret MIC from its onset to completion.
... Though the dark oxidation of Fe(II) and S compounds appeared to be less important compared with other aerobic and anaerobic metabolisms, typical representatives were abundant and may play a decisive role in corrosion and tubercle formation. Under pH-neutral to alkaline conditions, at high O 2 concentrations, abiotic Fe(II) oxidation is fast (Emerson, 2018). However, at low O 2 concentrations within the tubercle microaerophilic Fe(II) oxidizers, such as Leptothrix and Gallionella, could thrive promoting Fe(II) oxidation and Fe(III) (oxyhydr)oxide precipitation on their extracellular polymers. ...
... Tube-like structures were closely associated with diatoms suggesting a possible interaction of mixotrophic Fe(II)-oxidizing bacteria and organic carbon releasing phototrophs. The occurrence of Gallionella and Leptothrix at corrosions sites and their contribution to tubercle formation have been reported for many different marine and freshwater systems (Emde et al., 1992;Emerson, 2018;Ray et al., 2010a). ...
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The extent of how complex natural microbial communities contribute to metal corrosion is still not fully resolved, especially not for freshwater environments. In order to elucidate the key processes, we investigated rust tubercles forming massively on sheet piles along the river Havel (Germany) applying a complementary set of techniques. In-situ microsensor profiling revealed steep gradients of O2 , redox potential and pH within the tubercle. Micro-computed tomography and scanning electron microscopy showed a multi-layered inner structure with chambers and channels and various organisms embedded in the mineral matrix. Using Mössbauer spectroscopy we identified typical corrosion products including electrically conductive iron (Fe) minerals. Determination of bacterial gene copy numbers and sequencing of 16S rRNA and 18S rRNA amplicons supported a densely populated tubercle matrix with a phylogenetically and metabolically diverse microbial community. Based on our results and previous models of physic(electro)chemical reactions, we propose here a comprehensive concept of tubercle formation highlighting the crucial reactions and microorganisms involved (such as phototrophs, fermenting bacteria, dissimilatory sulphate and Fe(III) reducers) in metal corrosion in freshwaters.
... Then, it was proven that the reddish-brown microgranules are formed of very fine crystallites of poorly organized lepidocrocite ( Figure 13). It was also found that selected marine sponges grow only in the presence of iron ions [80], which are supplied to waters mainly from atmospheric sediments [81], hydrothermal vents [82], marginal sediments [83], artificial fertilization [84], groundwater discharges [85], and biocorrosion of artificial metal structures and shipwrecks [5,33,86]. The source of iron ions due to the biocorrosion of corresponding metallic constructs in seawater is crucial, especially when sponges use them as the substrate for attachment and growth [87]. ...
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Marine sponges of the subclass Keratosa originated on our planet about 900 million years ago and represent evolutionarily ancient and hierarchically structured biological materials. One of them, proteinaceous spongin, is responsible for the formation of 3D structured fibrous skeletons and remains enigmatic with complex chemistry. The objective of this study was to investigate the interaction of spongin with iron ions in a marine environment due to biocorrosion, leading to the occurrence of lepidocrocite. For this purpose, a biomimetic approach for the development of a new lepidocrocite-containing 3D spongin scaffold under laboratory conditions at 24 • C using artificial seawater and iron is described for the first time. This method helps to obtain a new composite as "Iron-Spongin", which was characterized by infrared spectroscopy and thermogravimetry. Furthermore , sophisticated techniques such as X-ray fluorescence, microscope technique, and X-Ray diffraction were used to determine the structure. This research proposed a corresponding mechanism of lepidocrocite formation, which may be connected with the spongin amino acids functional groups. Moreover, the potential application of the biocomposite as an electrochemical dopamine sensor is proposed. The conducted research not only shows the mechanism or sensor properties of "Iron-spongin" but also opens the door to other applications of these multifunctional materials.
... Therefore, the corrosion behaviour of steel can vary in the presence of different microorganisms. Currently, most studies focus on steel corrosion caused by bacteria such as anaerobic SRB, aerobic Pseudomonas aeruginosa, and iron-oxidising bacteria (IOB) [10][11][12][13]. However, the presence of fungi has also been found to significantly influence metal corrosion, often accelerating the process [14,15]. ...
Microbiologically influenced corrosion (MIC) is a key factor that damages engineering materials in marine environments. One of the major concerns in this regard is the corrosion protection of stainless steel (SS) caused against fungal attacks. This study investigated the effect of ultraviolet (UV) irradiation and benzalkonium chloride (BKC) on the corrosion of 316L stainless steel (316L SS) induced by marine Aspergillus terreus in 3.5 wt% NaCl solution. This was accomplished by employing microstructural characterisations and electrochemical analysis to analyse the synergistic inhibition behaviour of the two methods. The results indicated that while UV and BKC demonstrated individual abilities to suppress the biological activity of A. terreus, their inhibitory effects were not significant. The combination of UV light and BKC was found to cause a further decline in the biological activity of A. terreus. The analysis revealed that the combination of BKC and UV significantly decreased the sessile cell counts of A. terreus by more than three orders of magnitude. The fungal corrosion inhibition effect of individual application of UV light or BKC did not yield satisfactory results owing to the low intensity of UV and low concentration of BKC. Furthermore, the corrosion inhibition of UV and BKC occurred mainly during the early stages. The corrosion rate of the 316L SS declined rapidly when the combination of UV light and BKC were used, indicating that UV light and BKC exert a good synergistic inhibitory effect on the corrosion of the 316L SS caused by A. terreus. Therefore, the results suggest that the combination of UV light and BKC can be an effective approach to control the MIC of 316L SS in marine environments.
... The information provided by the modern complex community analysis of microbial corrosion cases shows that there are a range of microbes present that may affect corrosion processes. A recent review provides a long list of different microbes that accelerate iron corrosion [15], while iron oxidising bacteria [16], sulfate oxidising bacteria [17][18][19], metal depositing bacteria [20], archaea [21,22] and fungi [23] have also shown the ability to degrade metals. Hence, testing for the presence of SRB alone is not a definitive method for determining the likelihood of MIC occurring or if observed corrosion is due to MIC. ...
Conference Paper
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Interest in, and the general recognition of, microbially influenced corrosion (MIC) as an important form of structural degradation has rapidly increased over the last few decades. In this presentation I will reflect on key points I raised when I first started working on this topic approximately 16 years ago and discuss what, if anything, has changed since then. This will include several examples of MIC research undertaken by the teams that I have collaborated in over the years. Finally, I will provide some comments on future opportunities in MIC research: there's so much more to do on this exciting and challenging form of corrosion!
The uranium inventory in the Boeun aquifer is situated near an artificial reservoir (40-70 m apart) intended to supply water to nearby cities. However, toxic radionuclides can enter the reservoir. To determine the U mobility in the system, we analyzed groundwater and fracture-filling materials (FFMs) for environmental tracers, including microbial signatures, redox-sensitive elements and isotopes. In the site, U mass flux ranged from only 9.59 × 10-7 µg/L/y to 1.70 × 10-4 µg/L/y. The δ18O-H2O and 14C signatures showed that groundwater originated mainly from upland recharges and was not influenced by oxic surface water. We observed U accumulations (∼157 mg/kg) in shallow FFMs and Fe enrichments (∼226798 mg/kg) and anomalies in the 230Th/238U activity ratio (AR), 230Th/234U AR, δ56Fe and δ57Fe isotopes, suggesting that low U mobility in shallow depths is associated with a Fe-rich environment. At shallow depths, anaerobic Fe-oxidizers, Gallionella was prevalent in the groundwater, while Acidovorax was abundant near the U ore deposit depth. The Fe-rich environment at shallow depths was formed by sulfide dissolution, as demonstrated by δ34S-SO4 and δ18O-SO4 distribution. Overall, the Fe-rich aquifer including abundant sulfide minerals immobilizes dissolved U through biotic and abiotic processes, without significant leaching into nearby reservoirs.
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Iron oxidizing Zetaproteobacteria are well-known to colonize deep-sea hydrothermal vent fields around the world where iron-rich fluids are discharged into oxic seawater. How inter-field and intra-field differences in geochemistry influence the diversity of Zetaproteobacteria, however, remains largely unknown. Here, we characterize Zetaproteobacteria phylogenomic diversity, metabolic potential, and morphologies of the iron oxides they form, with a focus on the recently discovered Fåvne vent field. Located along the Mohns ridge in the Arctic, this vent field is a unique study site with vent fluids containing both iron and hydrogen with thick iron microbial mats (Fe mats) covering porously venting high-temperature (227-267 °C) black smoker chimneys. Through genome-resolved metagenomics and microscopy, we demonstrate that the Fe mats at Fåvne are dominated by tubular iron oxide sheaths, likely produced by Zetaproteobacteria of genus Ghiorsea . With these structures, Ghiorsea may provide a surface area for members of other abundant taxa such as Campylobacterota, Gammaproteobacteria and Alphaproteobacteria. Furthermore, Ghiorsea likely oxidizes both iron and hydrogen present in the fluids, with several Ghiorsea populations co-existing in the same niche. Homologues of Zetaproteobacteria Ni,Fe hydrogenases and iron oxidation gene cyc2 were found in genomes of other community members, suggesting exchange of these genes could have happened in similar environments. Our study provides new insights into Zetaproteobacteria in hydrothermal vents, their diversity, energy metabolism and niche formation. Importance Knowledge on microbial iron oxidation is important for understanding the cycling of iron, carbon, nitrogen, nutrients, and metals. The current study yields important insights into the niche sharing, diversification, and Fe(III) oxyhydroxide morphology of Ghiorsea , an iron- and hydrogen oxidizing Zetaproteobacteria representative belonging to ZetaOTU9. The study proposes that Ghiorsea exhibits a more extensive morphology of Fe(III) oxyhydroxide than previously observed. Overall, the results increase our knowledge on potential drivers of Zetaproteobacteria diversity in iron microbial mats and can eventually be used to develop strategies for the cultivation of sheath-forming Zetaproteobacteria.
Potentially corrosion-active microorganisms isolated from structural materials with the signs of biofouling on the coast of Kislaya Bay (Barents Sea, Russia) were studied: sulfate-reducing, iron-oxidizing and sulfur-oxidizing bacteria. The cultures of sulfate-reducing bacteria (Desulfovibrio sp., Halodesulfovibrio sp.), sulfur-oxidizing bacteria (Dietzia sp.), and iron-oxidizing bacteria (Pseudomonas fluorescens, Bacillus sp.) were identified on the basis of determining the nucleotide sequences of the 16S rRNA gene. The methods of scanning electron microscopy, energy dispersive microanalysis of the chemical composition, and powder X-ray diffraction analysis revealed significant changes in the structure and chemical composition of the surface layer of steel reinforcement samples exposed for 28 days in the presence of isolated microorganisms that demonstrated their active participation in corrosion processes. It has been shown that the formation of mineral analogues in corrosion products depends on the strains of studied bacteria and the peculiarities of their metabolism. Sulfate-reducing bacteria isolated from the littoral zone of the Barents Sea showed the highest activity in the development of corrosion processes.
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Iron (Fe) oxidation is one of Earth’s major biogeochemical processes, key to weathering, soil formation, water quality, and corrosion. However, our understanding of microbial contribution is limited by incomplete knowledge of microbial iron oxidation mechanisms, particularly in neutrophilic iron-oxidizers. The genomes of many, diverse iron-oxidizers encode a homolog to an outer-membrane cytochrome (Cyc2) shown to oxidize iron in two acidophiles. Phylogenetic analyses show Cyc2 sequences from neutrophiles cluster together, suggesting a common function, though this function has not been verified in these organisms. Therefore, we investigated the iron oxidase function of heterologously expressed Cyc2 from a neutrophilic iron-oxidizer Mariprofundus ferrooxydans PV-1. Cyc2PV-1 is capable of oxidizing iron, and its redox potential is 208 ± 20 mV, consistent with the ability to accept electrons from Fe ²⁺ at neutral pH. These results support the hypothesis that Cyc2 functions as an iron oxidase in neutrophilic iron-oxidizing organisms. Sequence analysis and modeling reveal the entire Cyc2 family share a unique fused cytochrome-porin structure, with a defining consensus motif in the cytochrome region. Based on structural analyses, we predict that the monoheme cytochrome Cyc2 specifically oxidizes dissolved Fe ²⁺ , in contrast to multiheme iron oxidases, which may oxidize solid Fe(II). With our results, there is now functional validation for diverse representatives of Cyc2 sequences. We present a comprehensive Cyc2 phylogenetic tree and offer a roadmap for identifying cyc2/ Cyc2 homologs and interpreting their function. The occurrence of cyc2 in many genomes beyond known iron-oxidizers presents the possibility that microbial iron oxidation may be a widespread metabolism. Importance Iron is practically ubiquitous across Earth’s environments, central to both life and geochemical processes, which depend heavily on the redox state of iron. Although iron oxidation, or “rusting,” can occur abiotically at near neutral pH, we find neutrophilic iron-oxidizing bacteria (FeOB) are widespread, including in aquifers, sediments, hydrothermal vents, pipes, and water treatment systems. FeOB produce highly reactive Fe(III) oxyhydroxides that bind a variety of nutrients and toxins, thus these microbes are likely a controlling force in iron and other biogeochemical cycles. There has been mounting evidence that Cyc2 functions as an iron oxidase in neutrophiles, but definitive proof of its function has long eluded us. This work provides conclusive biochemical evidence of iron oxidation by Cyc2 from neutrophiles. Cyc2 is common to a wide variety of iron-oxidizers, including acidophilic and phototrophic iron-oxidizers, suggesting that this fused cytochrome-porin structure is especially well-adapted for iron oxidation.
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Metal corrosion is of worldwide concern because it is the cause of major economic losses, and because it creates significant safety issues. The mechanism of the corrosion process, as influenced by bacteria, has been studied extensively. However, the bacterial communities that create the biofilms that form on metals are complicated, and have not been well studied. This is why we sought to analyze the composition of bacterial communities living on steel structures, together with the influence of ecological factors on these communities. The corrosion samples were collected from rust layers on steel plates that were immersed in seawater for two different periods at Sanya and Xiamen, China. We analyzed the bacterial communities on the samples by targeted 16S rRNA gene (V3–V4 region) sequencing using the Illumina MiSeq. Phylogenetic analysis revealed that the bacteria fell into 13 phylotypes (similarity level = 97%). Proteobacteria, Firmicutes and Bacteroidetes were the dominant phyla, accounting for 88.84% of the total. Deltaproteobacteria, Clostridia and Gammaproteobacteria were the dominant classes, and accounted for 70.90% of the total. Desulfovibrio spp., Desulfobacter spp. and Desulfotomaculum spp. were the dominant genera and accounted for 45.87% of the total. These genera are sulfate-reducing bacteria that are known to corrode steel. Bacterial diversity on the 6 months immersion samples was much higher than that of the samples that had been immersed for 8 years (P < 0.001, Student’s t-test). The average complexity of the biofilms from the 8-years immersion samples from Sanya was greater than those from Xiamen, but not significantly so (P > 0.05, Student’s t-test). Overall, the data showed that the rust layers on the steel plates carried many bacterial species. The bacterial community composition was influenced by the immersion time. The results of our study will be of benefit to the further studies of bacterial corrosion mechanisms and corrosion resistance.
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Extracellular electron transfer (EET) is recognized as a key biochemical process in circumneutral pH Fe(II)-oxidizing bacteria (FeOB). In this study, we searched for candidate EET genes in 73 neutrophilic FeOB genomes, among which 43 genomes are complete or close-to-complete and the rest have estimated genome completeness ranging from 5 to 91%. These neutrophilic FeOB span members of the microaerophilic, anaerobic phototrophic, and anaerobic nitrate-reducing FeOB groups. We found that many microaerophilic and several anaerobic FeOB possess homologs of Cyc2, an outer membrane cytochrome c originally identified in Acidithiobacillus ferrooxidans. The “porin-cytochrome c complex” (PCC) gene clusters homologous to MtoAB/PioAB are present in eight FeOB, accounting for 19% of complete and close-to-complete genomes examined, whereas PCC genes homologous to OmbB-OmaB-OmcB in Geobacter sulfurreducens are absent. Further, we discovered gene clusters that may potentially encode two novel PCC types. First, a cluster (tentatively named “PCC3”) encodes a porin, an extracellular and a periplasmic cytochrome c with remarkably large numbers of heme-binding motifs. Second, a cluster (tentatively named “PCC4”) encodes a porin and three periplasmic multiheme cytochromes c. A conserved inner membrane protein (IMP) encoded in PCC3 and PCC4 gene clusters might be responsible for translocating electrons across the inner membrane. Other bacteria possessing PCC3 and PCC4 are mostly Proteobacteria isolated from environments with a potential niche for Fe(II) oxidation. In addition to cytochrome c, multicopper oxidase (MCO) genes potentially involved in Fe(II) oxidation were also identified. Notably, candidate EET genes were not found in some FeOB, especially the anaerobic ones, probably suggesting EET genes or Fe(II) oxidation mechanisms are different from the searched models. Overall, based on current EET models, the search extends our understanding of bacterial EET and provides candidate genes for future research.
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Chemosynthetic Fe-oxidizing communities are common at diffuse-flow hydrothermal vents throughout the world’s oceans. The foundational members of these communities are the Zetaproteobacteria, a class of Proteobacteria that is primarily associated with ecosystems fueled by ferrous iron, Fe(II). We report here the discovery of two new isolates of Zetaproteobacteria isolated from the Mid-Atlantic Ridge (TAG-1), and the Mariana back-arc (SV-108), that are unique in that they can utilize either Fe(II) or molecular hydrogen (H2) as sole electron donor and oxygen as terminal electron acceptor for growth. Both strains precipitated Fe-oxyhydroxides as amorphous particulates. The cell doubling time on H2 vs Fe(II) for TAG-1 was 14.1 vs 21.8 h, and for SV-108 it was 16.3 vs 20 h, and it appeared both strains could use either H2 or Fe(II) simultaneously. The strains were close relatives, based on genomic analysis, and both possessed genes for the uptake NiFe-hydrogenase required for growth on H2. These two strains belong to Zetaproteobacteria operational taxonomic unit 9 (ZetaOTU9). A meta-analysis of public databases found ZetaOTU9 was only associated with Fe(II)-rich habitats, and not in other environments where known H2-oxidizers exist. These results expand the metabolic repertoire of the Zetaproteobacteria, yet confirm that Fe(II) metabolism is the primary driver of their physiology and ecology.
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The Epsilonproteobacteria is the fifth validly described class of the phylum Proteobacteria, known primarily for clinical relevance and for chemolithotrophy in various terrestrial and marine environments, including deep-sea hydrothermal vents. As 16S rRNA gene repositories have expanded and protein marker analysis become more common, the phylogenetic placement of this class has become less certain. A number of recent analyses of the bacterial tree of life using both 16S rRNA and concatenated marker gene analyses have failed to recover the Epsilonproteobacteria as monophyletic with all other classes of Proteobacteria. In order to address this issue, we investigated the phylogenetic placement of this class in the bacterial domain using 16S and 23S rRNA genes, as well as 120 single-copy marker proteins. Single- and concatenated-marker trees were created using a data set of 4,170 bacterial representatives, including 98 Epsilonproteobacteria. Phylogenies were inferred under a variety of tree building methods, with sequential jackknifing of outgroup phyla to ensure robustness of phylogenetic affiliations under differing combinations of bacterial genomes. Based on the assessment of nearly 300 phylogenetic tree topologies, we conclude that the continued inclusion of Epsilonproteobacteria within the Proteobacteria is not warranted, and that this group should be reassigned to a novel phylum for which we propose the name Epsilonbacteraeota (phyl. nov.). We further recommend the reclassification of the order Desulfurellales (Deltaproteobacteria) to a novel class within this phylum and a number of subordinate changes to ensure consistency with the genome-based phylogeny. Phylogenomic analysis of 658 genomes belonging to the newly proposed Epsilonbacteraeota suggests that the ancestor of this phylum was an autotrophic, motile, thermophilic chemolithotroph that likely assimilated nitrogen from ammonium taken up from the environment or generated from environmental nitrate and nitrite by employing a variety of functional redox modules. The emergence of chemoorganoheterotrophic lifestyles in several Epsilonbacteraeota families is the result of multiple independent losses of various ancestral chemolithoautotrophic pathways. Our proposed reclassification of this group resolves an important anomaly in bacterial systematics and ensures that the taxonomy of Proteobacteria remains robust, specifically as genome-based taxonomies become more common.
The biogeochemical cycle of iron is intricately linked to numerous element cycles. Although biological processes that catalyze the reductive side of the iron cycle are established, little is known about microbial oxidative processes on iron cycling in sedimentary environments-resulting in the formation of iron oxides. Here we show that a potential source of sedimentary iron oxides originates from the metabolic activity of iron-oxidizing bacteria from the class Zetaproteobacteria, presumably enhanced by burrowing animals in coastal sediments. Zetaproteobacteria were estimated to be a global total of 1026 cells in coastal, bioturbated sediments, and predicted to annually produce 8 × 1015 g of Fe in sedimentary iron oxides-55 times larger than the annual flux of iron oxides deposited by rivers. These data suggest that iron-oxidizing Zetaproteobacteria are keystone organisms in marine sedimentary environments-despite their low numerical abundance-yet exert a disproportionate impact via the rejuvenation of iron oxides.
The term microbiologically influenced corrosion (MIC) is used to designate corrosion due to the presence and activities of microorganisms, that is, those organisms that cannot be seen individually with the unaided human eye. Information in this chapters related to internal MIC is limited to petroleum-based hydrocarbon fuels in low-alloy steel piping. The focus of most testing, monitoring, and research related to MIC in the oil and gas industry for internal and external pipeline surfaces is on sulfate-reducing bacteria (SRB). Consequently, any discussion of causative microorganisms, in the chapter, is dominated by references to SRB. Microorganisms have developed several strategies for survival in natural environments: (1) spore formation (2) biofilm formation (3) dwarf cells, and (4) a viable, but non-culturable state. Pitting is the typical type of internal corrosion in pipelines. All line pipe is externally coated and can be further protected with cathodic protection (CP).
Iron (Fe) oxides/oxyhydroxides in drinking water distribution systems (DWDS), produced by electrochemical, chemical, and biological reactions, can adsorb toxic metal ions, including strontium, lead, arsenic, and vanadium that, if desorbed, generate pulses of drinking water with elevated toxic metal ion concentrations. To illustrate that potential, sorption data for strontium ( cation) and vanadium (oxyanion) in functioning DWDS are reviewed. In addition, the influence of flow/no flow on adsorption and desorption of strontium in a model DWDS is included. The reactions that influence adsorption and desorption within a DWDS are extremely complicated and poorly understood. The sorption capacity of Fe oxhydroxides varies with surface area, which in turn varies with source water and disinfectant. Desorption and release can be triggered by changes in source water, disinfection chemicals, or flow. Because of the interrelatedness of adsorption/desorption and Fe corrosion products, subtle changes in DWDS operating procedures can trigger major changes in water quality.
The authors examined the physiochemical and microbiological properties of archived rusticles from World War II shipwrecks in the Gulf of Mexico. Rusticles, iron (Fe)-rich accumulations on shipwrecks in marine environments, have long been assumed to be the result of low alloy steel corrosion. In many cases the assumed corrosion has been attributed to biodeterioration because of the presence of specific types of bacteria associated with the rusticles. However, archived rusticles from WWII shipwrecks in the Gulf of Mexico (GOM) do not have the mineralogical layering typical of iron corrosion products. Moreover, spatial relationships between bacteria and rusticles cannot be interpreted as biodeterioration. The authors concluded that environmental Fe plays a role in rusticle formation and differences in Fe concentrations can be used to explain differences in rusticle size and distribution with depth in the GOM. Both biotic and abiotic mechanisms for Fe accumulation are provided.
Sulfide mineral precipitation occurs at mid-ocean ridge (MOR) spreading centers, both in the form of plume particles and seafloor massive sulfide structures. A common constituent of MOR is the iron-bearing sulfide mineral pyrrhotite, which was chosen as a substrate for in-situ incubation studies in shallow waters of Catalina Island, CA to investigate the colonization of iron-oxidizing bacteria. Microbial community datasets were obtained from in-situ incubated pyrrhotite, allowing for direct comparison to microbial communities of iron-sulfides from active and inactive chimneys in deep-sea environments. Unclassified Gammaproteobacteria and Alphaproteobacteria (Magnetovibrio) largely dominated the bacterial community on pyrrhotite samples incubated in the water column while samples incubated at the surface sediment showed more even dominance by Deltaproteobacteria (Desulfobulbus), Gammaproteobacteria (Piscirickettsiaceae), Alphaproteobacteria (Rhodobacteraceae), and Bacteroidetes (Flavobacteriia). Cultivations that originated from pyrrhotite samples resulted in the enrichment of both, sheath-forming and stalk-forming Zetaproteobacteria. Additionally, a putative novel species of Thiomicrospira was isolated and shown to grow autotrophically with iron, indicating a new biogeochemical role for this ubiquitous microorganism. This article is protected by copyright. All rights reserved.