Iron Bacteria

Iron-oxidizing bacteria are chemotrophic bacteria that derive energy by oxidizing dissolved ferrous 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.

Iron is a very important 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 in the Earth's crust, soil, and sediments. Iron is a trace element in marine environments. Its role in the metabolism of some chemolithotrophs is probably very ancient.

As Liebig's law of the minimum notes, the essential element present in the smallest amount (called limiting factor) is the one that determines the growth rate of a population. Iron is the most common limiting element in phytoplankton communities and has a key role in structuring and determining their abundance. It is particularly important in the high-nutrient, low-chlorophyll regions, where the presence of micronutrients is mandatory for the total primary production.

Introduction

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 (5.4%) in comparison to manganese (0.1%) 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.

Habitat and iron-oxidizing bacterial groups

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 (hydrothermal vents, deep ocean basalts, groundwater iron seeps) 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(II) 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.

Despite being phylogenetically diverse, the microbial ferrous iron oxidation metabolic strategy (found in Archaea and Bacteria) is present in 7 phyla, being highly pronounced in the phylum Pseudomonadota (formerly Proteobacteria), 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 Nitrosospirota 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 iron-oxidizing bacteria. This biosignature has been a tool to understand the importance of iron metabolism in the Earth's past.

Ferrous iron oxidation and early life

Unlike most lithotrophic metabolisms, the oxidation of Fe²⁺ to Fe³⁺ yields very little energy to the cell (∆G° = 29 kJ/mol and ∆G° = -90 kJ/mol in acidic and neutral environments, respectively) 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 (through the excretion of twisted stalks). The aerobic iron-oxidizing bacterial metabolism is thought to have made a remarkable contribution to the formation of the largest iron deposit ( banded iron formation (BIF)) due to the advent of oxygen in the atmosphere 2.7 billion years ago (produced by cyanobacteria).

However, with the discovery of Fe(II) oxidation carried out under anoxic conditions in the late 1990s using light as an energy source or chemolithotrophically, using a different terminal electron acceptor (mostly NO₃⁻), 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(III) reducers, they may have been responsible for the BIF in the Precambrian eon.

Microbial ferrous iron oxidation metabolism

Anoxygenic phototrophic ferrous iron oxidation

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 (or rTCA cycle) in a neutrophilic environment (pH 5.5-7.2), producing Fe³⁺ oxides as a waste product that precipitates as a mineral, according to the following stoichiometry (4 mM of Fe(II) can yield 1 mM of CH₂O):

(∆G° > 0)

Nevertheless, some bacteria do not use the photoautotrophic Fe(II) oxidation metabolism for growth purposes. Instead, it has been suggested that these groups are sensitive to Fe(II) and therefore oxidize Fe(II) into more insoluble Fe(III) oxide to reduce its toxicity, enabling them to grow in the presence of Fe(II). On the other hand, based on experiments with ''R. capsulatus'' SB1003 (photoheterotrophic), it has been demonstrated that the oxidation of Fe(II) might be the mechanisms whereby the bacteria is enable to access organic carbon sources (acetate, succinate) whose use depends on Fe(II) oxidation Nonetheless, many iron-oxidizing bacteria can use other compounds as electron donors in addition to Fe(II), or even perform dissimilatory Fe(III) 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 lighted regions (near the surface) 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(II) oxidation deeper in the sediment/water column, with low light availability.

Nitrate-dependent Fe(II) oxidation

Light penetration can limit the Fe(II) oxidation in the water column. However, nitrate dependent microbial Fe(II) oxidation is a light independent metabolism that has been shown to support microbial growth in various freshwater and marine sediments (paddy soil, stream, brackish lagoon, hydrothermal, deep-sea sediments) and later on demonstrated as a pronounced metabolism within the water column at the OMZ. Microbes that perform this metabolism are successful in neutrophilic or alcaline environments, due to the high difference in between the redox potential of the couples Fe²⁺/Fe³⁺ and NO₃⁻/NO₂⁻ (+200 mV and +770 mV, respectively) releasing a lot of free energy when compared to other iron oxidation metabolisms

(∆G°=-103.5 kJ/mol)

The microbial oxidation of ferrous iron coupled to denitrification (with nitrite or dinitrogen gas being the final product) can be autotrophic using inorganic carbon or organic co-substrates (acetate, butyrate, pyruvate, ethanol) 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.

Ferrous iron oxidizers in the marine environment

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