Iron-oxidizing bacteria

Iron-oxidizing bacteria are chemotrophic bacteria that derive energy by oxidizing dissolved iron. They are known to grow and proliferate in waters containing iron concentrations as low as 0.1 mg/L. However, at least 0.3 ppm of dissolved oxygen is needed to carry out the oxidation.
When de-oxygenated water reaches a source of oxygen, iron bacteria convert dissolved iron into an insoluble reddish-brown gelatinous slime that discolors stream beds and can stain plumbing fixtures, clothing, or utensils washed with the water carrying it.
Organic material dissolved in water is often the underlying cause of an iron-oxidizing bacteria population. Groundwater may be naturally de-oxygenated by decaying vegetation in swamps. Useful mineral deposits of bog iron ore have formed where groundwater has historically emerged and been exposed to atmospheric oxygen. Anthropogenic hazards like landfill leachate, septic drain fields, or leakage of light petroleum fuels like gasoline are other possible sources of organic materials allowing soil microbes to de-oxygenate groundwater.
A similar reaction may form black deposits of manganese dioxide from dissolved manganese but is less common because of the relative abundance of iron in comparison to manganese in average soils. The sulfurous smell of rot or decay sometimes associated with iron-oxidizing bacteria results from the enzymatic conversion of soil sulfates to volatile hydrogen sulfide as an alternative source of oxygen in anaerobic water.
Iron is a very important chemical element required by living organisms to carry out numerous metabolic reactions such as the formation of proteins involved in biochemical reactions. Examples of these proteins include iron–sulfur proteins, hemoglobin, and coordination complexes. Iron has a widespread distribution globally and is considered one of the most abundant elements in the Earth's crust, soil, and sediments. Iron is a trace element in marine environments. Its role as the electron donor of some chemolithotrophs is probably very ancient.

Metabolism

The anoxygenic phototrophic iron oxidation was the first anaerobic metabolism to be described within the iron anaerobic oxidation metabolism. The photoferrotrophic bacteria use Fe²⁺ as electron donor and the energy from light to assimilate CO₂ into biomass through the Calvin Benson-Bassam cycle in a neutrophilic environment, producing Fe³⁺ oxides as a waste product that precipitates as a mineral, according to the following stoichiometry :

Nevertheless, some bacteria do not use the photoautotrophic Fe oxidation metabolism for growth purposes. Instead, it has been suggested that these groups are sensitive to Fe and therefore oxidize Fe into more insoluble Fe oxide to reduce its toxicity, enabling them to grow in the presence of Fe. On the other hand, based on experiments with Rhodobacter capsulatus SB1003, it has been demonstrated that the oxidation of Fe might be the mechanisms whereby the bacteria are enabled to access organic carbon sources whose use depends on Fe oxidation. Nonetheless, many iron-oxidizing bacteria can use other compounds as electron donors in addition to Fe, or even perform dissimilatory Fe reduction as the Geobacter metallireducens.
The dependence of photoferrotrophics on light as a crucial resource can take the bacteria to a cumbersome situation where, due to their requirement for anoxic illuminated regions, they could be faced with competition by abiotic reactions due to the presence of molecular oxygen. To avoid this problem, they tolerate microaerophilic surface conditions or perform the photoferrotrophic Fe oxidation deeper in the sediment/water column, with low light availability.
Light penetration can limit the Fe oxidation in the water column. However, nitrate dependent microbial Fe oxidation is a light independent metabolism that has been shown to support microbial growth in various freshwater and marine sediments and later on demonstrated as a pronounced metabolism within the water column at the oxygen minimum zone. Microbes that perform this metabolism are successful in neutrophilic or alkaline environments, due to the high difference between the redox potential of the couples Fe²⁺/Fe³⁺ and NO₃⁻/NO₂⁻ releasing a lot of free energy when compared to other iron oxidation metabolisms.

The microbial oxidation of ferrous iron coupled to denitrification can be autotrophic using inorganic carbon, or organic co-substrates performing heterotrophic growth in the absence of inorganic carbon. It has been suggested that the heterotrophic nitrate-dependent ferrous iron oxidation using organic carbon might be the most favorable process. This metabolism might be very important for carrying out an important step in the biogeochemical cycle within the OMZ.

Types

The microbial ferrous iron oxidation metabolic strategy is present in 7 phyla, being highly pronounced in the phylum Pseudomonadota, particularly the Alpha, Beta, Gamma, and Zetaproteobacteria classes, and among the Archaea domain in the "Euryarchaeota" and Thermoproteota phyla, as well as in Actinomycetota, Bacillota, Chlorobiota, and Nitrospirota phyla.
There are very well-studied iron-oxidizing bacterial species such as Thiobacillus ferrooxidans, and Leptospirillum ferrooxidans, and some like Gallionella ferruginea and Mariprofundis ferrooxydans are able to produce a particular extracellular stalk-ribbon structure rich in iron, known as a typical biosignature of microbial iron oxidation. These structures can be easily detected in a sample of water, indicating the presence of iron-oxidizing bacteria. This biosignature has been a tool to understand the importance of iron metabolism in the Earth's past.

Habitat

Iron-oxidizing bacteria colonize the transition zone where de-oxygenated water from an anaerobic environment flows into an aerobic environment. Groundwater containing dissolved organic material may be de-oxygenated by microorganisms feeding on that dissolved organic material. In aerobic conditions, pH variation plays an important role in driving the oxidation reaction of Fe²⁺/Fe³⁺. At neutrophilic pHs the oxidation of iron by microorganisms is highly competitive with the rapid abiotic reaction occurring in <1 min. Therefore, the microbial community has to inhabit microaerophilic regions where the low oxygen concentration allows the cell to oxidize Fe and produce energy to grow. However, under acidic conditions, where ferrous iron is more soluble and stable even in the presence of oxygen, only biological processes are responsible for the oxidation of iron, thus making ferrous iron oxidation the major metabolic strategy in iron-rich acidic environments.
In the marine environment, the most well-known class of iron oxidizing-bacteria is zetaproteobacteria, which are major players in marine ecosystems. Being generally microaerophilic they are adapted to live in transition zones where the oxic and anoxic waters mix. The zetaproteobacteria are present in different Fe-rich habitats, found in deep ocean sites associated with hydrothermal activity and in coastal and terrestrial habitats, and have been reported in the surface of shallow sediments, beach aquifer, and surface water.
Mariprofundus ferrooxydans is one of the most common and well-studied species of zetaproteobacteria. It was first isolated from the Kamaʻehuakanaloa Seamount vent field, near Hawaii at a depth between 1100 and 1325 meters, on the summit of this shield volcano. Vents can be found ranging from slightly above ambient to high temperature. The vent waters are rich in CO₂, Fe and Mn. Large, heavily encrusted mats with a gelatinous texture are created by iron-oxidizing bacteria as a by-product, and can be present around the vent orifices. The vents present at Kamaʻehuakanaloa seamount can be categorized into two types based on concentration and temperature of flow. Those with a focused and high-temperature flow can be expected to show higher flow rates as well. These vents are characterized by flocculent mats aggregated around the vent orifices. Mat depth at focused, high-temperature vents averages in the tens of centimeters, but can vary. In contrast, vents with cooler and diffuse flow can create mats up to one meter thick. These mats may cover hundreds of square meters of sea floor. Either type of mat can be colonized by other bacterial communities, which can change the chemical composition and the flow of the local waters.

Impact on early life on Earth

Unlike most lithotrophic metabolisms, the oxidation of Fe²⁺ to Fe³⁺ yields very little energy to the cell compared to other chemolithotrophic metabolisms. Therefore, the cell must oxidize large amounts of Fe²⁺ to fulfill its metabolic requirements while contributing to the mineralization process. The aerobic iron-oxidizing bacterial metabolism is thought to have made a remarkable contribution to the formation of the largest iron deposit due to the advent of oxygen in the atmosphere 2.7 billion years ago.
However, with the discovery of Fe oxidation carried out under anoxic conditions in the late 1990s using light as an energy source or chemolithotrophically, using a different terminal electron acceptor, the suggestion arose that anoxic Fe²⁺ metabolism may pre-date aerobic Fe²⁺ oxidation and that the age of the BIF pre-dates oxygenic photosynthesis. This suggests that microbial anoxic phototrophic and anaerobic chemolithotrophic metabolism may have been present on the ancient earth, and together with Fe reducers, they may have been responsible for the BIF in the Precambrian eon.

Impact of climate change

In open ocean systems full of dissolved iron, iron-oxidizing bacterial metabolism is ubiquitous and influences the iron cycle. Nowadays, this biochemical cycle is undergoing modifications due to pollution and climate change; nonetheless, the normal distribution of ferrous iron in the ocean could be affected by global warming under the following conditions: acidification, shifting of ocean currents, and ocean water and groundwater hypoxia trend.
These are all consequences of the substantial increase of CO₂ emissions into the atmosphere from anthropogenic sources. Currently the concentration of carbon dioxide in the atmosphere is around 420 ppm, and about a quarter of the total CO₂ emission enters the oceans. Reacting with seawater it produces bicarbonate ion and thus the ocean acidity increases. Furthermore, the temperature of the ocean has increased by almost one degree causing the melting of big quantities of glaciers contributing to the sea-level rise. This lowers the O₂ solubility by inhibiting the oxygen exchange between surface waters, where O₂ is very abundant, and anoxic deep waters.
All these changes in the marine parameters impact the iron biogeochemical cycle and could have several and critical implications on ferrous iron oxidizing microbes; hypoxic and acid conditions could improve primary productivity in the superficial and coastal waters because that would increase the availability of ferrous iron Fe for microbial iron oxidation. Still, at the same time, this scenario could also disrupt the cascade effect to the sediment in deep water and cause the death of benthonic animals. Moreover it is very important to consider that iron and phosphate cycles are strictly interconnected and balanced, so that a small change in the first could have substantial consequences on the second.