The class Zetaproteobacteria is the sixth and most recently described class of the Proteobacteria. Zetaproteobacteria can also refer to the group of organisms assigned to this class. The Zetaproteobacteria are represented by a single described species, Mariprofundus ferrooxydans, which is an iron-oxidizing neutrophilic chemolithoautotroph originally isolated from Loihi Seamount in 1996 (post-eruption). Molecular cloning techniques focusing on the small subunit ribosomal RNA gene have also been used to identify a more diverse majority of the Zetaproteobacteria that have as yet been unculturable.
Regardless of culturing status, the Zetaproteobacteria show up worldwide in estuarine and marine habitats associated with opposing steep redox gradients of reduced (ferrous) iron and oxygen, either as a minor detectable component or as the dominant member of the microbial community. Zetaproteobacteria have been most commonly found at deep-sea hydrothermal vents, though recent discovery of members of this class in near-shore environments has led to the reevaluation of Zetaproteobacteria distribution and significance.
As potentially an entire class of marine iron oxidizers, the Zetaproteobacteria play a substantial role in biogeochemical cycling, both past and present. Ecologically, the Zetaproteobacteria play a major role in the engineering of their own environment through the use of the controlled deposition of mineralized iron oxides, also directly affecting the environment of other members of the microbial community.
Prevalence of the Zetaproteobacteria in near-shore metal (e.g. steel) coupon biocorrosion experiments highlights the impact of these marine iron oxidizers on expensive problems such as the rusting of ship hulls, metal pilings, and pipelines.
The Zetaproteobacteria were first discovered in 1991 by Craig Moyer, Fred Dobbs, and David Karl as a single rare clone in a mesophilic, or moderate temperature, hydrothermal vent field known as Pele's Vents at Loihi Seamount, Hawaii. This particular vent was dominated by sulfur-oxidizing Epsilonproteobacteria. With no close relatives known at the time, the clone was initially labeled as a Gammaproteobacteria.
Subsequent isolation of two strains of M. ferrooxydans, PV-1 and JV-1, along with the increasing realization that a phylogenetically distinct group of Proteobacteria (the Zetaproteobacteria) could be found globally as dominant members of bacterial communities led to the suggestion for the creation of this new class of the Proteobacteria.
One of the most distinctive ways of identifying circumneutral iron oxidizing bacteria visually is by identifying the structure of the mineralized iron oxyhydroxide product created during iron oxidation. Oxidized, or ferric iron is insoluble at circumneutral pH, thus the microbe must have a way of dealing with the mineralized "waste" product. It is thought that one method to accomplish this is to control the deposition of oxidized iron. Some of the most common morphotypes include: amorphous particulate oxides, twisted or helical stalks (figure), sheaths, and y-shaped irregular filaments.
These morphologies exist both in freshwater and marine iron habitats, though common freshwater iron-oxidizing bacteria such as Gallionella sp. (twisted stalk) and Leptothrix ochracea (sheath) have only extremely rarely been found in the deep sea (not significant abundance). The only currently published morphotype that has been partially resolved is the twisted stalk, which is commonly formed by M. ferrooxydans. This bacteria is a gram negative kidney-bean-shaped cell that deposits iron oxides on the concave side of the cell, forming twisted stalks as it moves through its environment.
Iron oxidation morphotypes can be preserved and have been detected in ancient hydrothermal deposits.
An operational taxonomic unit, or an OTU, allows a microbiologist to define a bacterial taxa using defined similarity bins based on a gene of interest. In microbial ecology, the small subunit ribosomal RNA gene is generally used at a cut off of 97% similarity to define an OTU. In the most basic sense, the OTU represents a bacterial species.
For the Zetaproteobacteria, 28 OTUs have been defined. Of interest were the two globally distributed OTUs that dominated the phylogenetic tree, two OTUs that seemed to originate in the deep subsurface, and several endemic OTUs, along with the relatively limited detection of the isolated Zetaproteobacteria representative.
- Deep-sea hydrothermal vents associated with:
- back arc spreading centers/troughs
- Island arcs
- Spreading centers (on- and off axis)
- Inactive sulfides along the East Pacific Rise (spreading center)
- Flooded caldera
- Guaymas Basin
- Brine/seawater interface
- Salt marsh sediment
- Near-shore metal biocorrosion experiments
- Rimicaris exoculata (shrimp) gut at the MAR
- Antarctica continental shelf sediment
All of the habitats where Zetaproteobacteria have been found have (at least) one thing in common: they all provide an interface of steep redox gradients of oxygen and iron.
Reduced hydrothermal fluids, for instance, exiting from vents in the deep-sea carry with them high concentrations of ferrous iron and other reduced chemical species, creating a gradient upward through a microbial mat of high to low ferrous iron. Similarly, oxygen from the overlying seawater diffuses into the microbial mat resulting in a downward gradient of high to low oxygen. Zetaproteobacteria are thought to live at the interface, where there is enough oxygen for use as an electron acceptor without there being too much oxygen for the organism to compete with the increased rate of chemical oxidation, and where there is enough ferrous iron for growth.
Iron oxidation is not always energetically favorable. Reference discusses favorable conditions for iron oxidation in habitats that otherwise may have been thought to be dominated by the more energy yielding metabolisms of hydrogen or sulfur oxidation.
Note: Iron is not the only reduced chemical species accociated with these redox gradient environments. It is likely that Zetaproteobacteria are not all iron oxidizers.
Iron oxidation pathways in both freshwater acidophilic and circumneutral iron oxidation habitats such as acid mine drainage or groundwater iron seeps, respectively, though not complete, are better understood than marine circumneutral iron oxidation.
The genome for the only described cultured representative of the Zetaproteobacteria was recently published, and while no definitive iron oxidation genes were identified, the gene neighborhood of a molybdopterin oxidoreductase protein was identified as a place to start looking at candidate iron oxidation pathway genes. Though M. ferrooxydans was isolated as an autotroph, able to fix carbon dioxide, the genome of PV-1 revealed an ability to grow mixotrophically on fructose or mannose.
It is difficult at this point to speculate on the metabolism of the entire class with the limited sample size.
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