Zetaproteobacteria | |
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Scientific classification | |
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Class: | Zetaproteobacteria Makita et al. 2017 |
Order: | Mariprofundales Makita et al. 2017 |
Family: | Mariprofundaceae Hördt et al. 2020 |
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The class Zetaproteobacteria is the sixth and most recently described class of the Pseudomonadota. [1] Zetaproteobacteria can also refer to the group of organisms assigned to this class. The Zetaproteobacteria were originally represented by a single described species, Mariprofundus ferrooxydans , [2] which is an iron-oxidizing neutrophilic chemolithoautotroph originally isolated from Kamaʻehuakanaloa Seamount (formerly Loihi) in 1996 (post-eruption). [1] [3] 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. [4]
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. [5] [6] [7] [8] [9] [10] Zetaproteobacteria have been most commonly found at deep-sea hydrothermal vents, [4] though recent discovery of members of this class in near-shore environments has led to the reevaluation of Zetaproteobacteria distribution and significance. [11] [12] [13]
The Zetaproteobacteria are distributed worldwide in deep sea and near shore environments at oxic/anoxic interfaces. With this wide distribution, the Zetaproteobacteria have the potential to 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. [11] [14] [15]
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 Kamaʻehuakanaloa Seamount (formerly Loihi), Hawaii. This particular vent was dominated by sulfur-oxidizing Campylobacterota. With no close relatives known at the time, the clone was initially labeled as Gammaproteobacteria. [16]
Subsequent isolation of two strains of M. ferrooxydans, PV-1 and JV-1, [3] along with the increasing realization that a phylogenetically distinct group of Pseudomonadota (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.
Neutrophilic microaerophilic Fe-oxidizing bacteria are typically cultivated using an agarose-stabilized or liquid culture with an FeS or FeCO3 plug. The headspace of the culture tube is then purged with air or a low concentration of oxygen (often 1% or less O2). Fe-oxidizers have also successfully been cultivated in liquid culture with FeCl2 as the Fe source. These cultivation techniques follow those found in Emerson and Floyd (2005). [17]
Recently, researchers have been able to culture the Zetaproteobacteria using graphite electrodes at a fixed voltage. [18] Researchers have also aimed to improve cultivation techniques using a high-biomass batch culturing technique. [19]
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. [3] [20] 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. [21] [22] [23] Some of the most common morphotypes include: amorphous particulate oxides, twisted or helical stalks (figure), [21] sheaths, [24] 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). One 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. [21] [22]
Another common Zetaproteobacteria morphotype is the sheath structure, which has yet to be isolated, but has been identified with fluorescence in situ hybridization (FISH). [24]
Iron oxidation morphotypes can be preserved and have been detected in ancient hydrothermal deposits preserved in the rock record. [25] [26] [27] [28] [29] Some current work is focused on how the Zetaproteobacteria form their individual biominerals in the modern environment so that scientists can better interpret Fe biominerals found in the rock record. [30] [31] [32]
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. [4] Of interest were the two globally distributed OTUs that dominated the phylogenetic tree, two OTUs that seemed to originate in the deep subsurface, [10] and several endemic OTUs, along with the relatively limited detection of the isolated Zetaproteobacteria representative.
Zetaproteobacteria OTUs can now be classified according to the naming scheme used in McAllister et al. (2011). [4] The program ZetaHunter uses closed reference binning to identify sequences closely related to the established OTUs in addition to identifying novel Zetaproteobacteria OTUs. ZetaHunter's feature list continues to grow, but includes: 1) stable OTU binning, 2) sample comparison, 3) database and mask management options, 4) multi-threaded processing, 5) chimera checking, 6) checks for non-database-related sequences, and 7) OTU network maps. The ZetaHunter software can be downloaded at: https://github.com/mooreryan/ZetaHunter
Phylogeny of Mariprofundaceae by GTDB 07-RS207 [33] [34] [35] | |||||||||||||||||||||||||||||||||
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All of the habitats where Zetaproteobacteria have been found have (at least) two things in common: 1) they all provide an interface of steep redox gradients of oxygen and iron. [66] & 2) they are marine or brackish. [47]
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. [20] [66]
Iron oxidation is not always energetically favorable. Reference [42] 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 acidophilic and circumneutral freshwater iron oxidation habitats, such as acid mine drainage or groundwater iron seeps, respectively, are better understood than marine circumneutral iron oxidation.
In recent years, researchers have made progress in suggesting possibilities for how the Zetaproteobacteria oxidize iron, primarily through comparative genomics. With this technique, genomes from organisms with similar function, for example the freshwater Fe-oxidizing Betaproteobacteria and the marine Fe-oxidizing Zetaproteobacteria, are compared to find genes that may be required for this function. Identifying the iron oxidation pathway in the Zetaproteobacteria began with the publication of the first described cultured representative, M. ferrooxydans strain PV-1. In this genome, the gene neighborhood of a molybdopterin oxidoreductase protein was identified as a place to start looking at candidate iron oxidation pathway genes. [67] In a follow-up analysis of a metagenomic sample, Singer et al. (2013) concluded that this molybdopterin oxidoreductase gene cassette was likely involved in Fe oxidation. [68] Comparative analysis of several single cell genomes, however, suggested an alternative conserved gene cassette with several cytochrome c and cytochrome oxidase genes to be involved in Fe oxidation. [69] For further reading on Fe oxidation pathways see reference. [70]
The phylogenetic distance between the Zetaproteobacteria and the Fe-oxidizing freshwater Betaproteobacteria suggests that Fe oxidation and the produced biominerals are the result of convergent evolution. [24] Comparative genomics has been able to identify several genes that are shared between the two clades, however, suggesting that the trait of Fe oxidation could have been horizontally transferred, possibly virally mediated. [71] [72]
Fe mats associated with the Zetaproteobacteria, in addition to oxidizing Fe have been found to have the genetic potential for denitrification, arsenic detoxification, Calvin-Benson-Bassham (CBB) cycle, and reductive tricarboxylic acid (rTCA) cycles. Novel primers have been designed to detect these genes in environmental samples. [73]
It is difficult at this point to speculate on the metabolism of the entire class of Zetaproteobacteria (with at least 28 different OTUs/species) with the limited sample size.
Riftia pachyptila, commonly known as the giant tube worm and less commonly known as the giant beardworm, is a marine invertebrate in the phylum Annelida related to tube worms commonly found in the intertidal and pelagic zones. R. pachyptila lives on the floor of the Pacific Ocean near hydrothermal vents. The vents provide a natural ambient temperature in their environment ranging from 2 to 30 °C, and this organism can tolerate extremely high hydrogen sulfide levels. These worms can reach a length of 3 m, and their tubular bodies have a diameter of 4 cm (1.6 in).
Kamaʻehuakanaloa Seamount is an active submarine volcano about 22 mi (35 km) off the southeast coast of the island of Hawaii. The top of the seamount is about 3,200 ft (975 m) below sea level. This seamount is on the flank of Mauna Loa, the largest shield volcano on Earth. Kamaʻehuakanaloa is the newest volcano in the Hawaiian–Emperor seamount chain, a string of volcanoes that stretches about 3,900 mi (6,200 km) northwest of Kamaʻehuakanaloa. Unlike most active volcanoes in the Pacific Ocean that make up the active plate margins on the Pacific Ring of Fire, Kamaʻehuakanaloa and the other volcanoes of the Hawaiian–Emperor seamount chain are hotspot volcanoes and formed well away from the nearest plate boundary. Volcanoes in the Hawaiian Islands arise from the Hawaii hotspot, and as the youngest volcano in the chain, Kamaʻehuakanaloa is the only Hawaiian volcano in the deep submarine preshield stage of development.
Sulfate-reducing microorganisms (SRM) or sulfate-reducing prokaryotes (SRP) are a group composed of sulfate-reducing bacteria (SRB) and sulfate-reducing archaea (SRA), both of which can perform anaerobic respiration utilizing sulfate (SO2−
4) as terminal electron acceptor, reducing it to hydrogen sulfide (H2S). Therefore, these sulfidogenic microorganisms "breathe" sulfate rather than molecular oxygen (O2), which is the terminal electron acceptor reduced to water (H2O) in aerobic respiration.
Ferroglobus is a genus of the Archaeoglobaceae.
The iron cycle (Fe) is the biogeochemical cycle of iron through the atmosphere, hydrosphere, biosphere and lithosphere. While Fe is highly abundant in the Earth's crust, it is less common in oxygenated surface waters. Iron is a key micronutrient in primary productivity, and a limiting nutrient in the Southern ocean, eastern equatorial Pacific, and the subarctic Pacific referred to as High-Nutrient, Low-Chlorophyll (HNLC) regions of the ocean.
The hydrogen cycle consists of hydrogen exchanges between biotic (living) and abiotic (non-living) sources and sinks of hydrogen-containing compounds.
Sulfur-reducing bacteria are microorganisms able to reduce elemental sulfur (S0) to hydrogen sulfide (H2S). These microbes use inorganic sulfur compounds as electron acceptors to sustain several activities such as respiration, conserving energy and growth, in absence of oxygen. The final product of these processes, sulfide, has a considerable influence on the chemistry of the environment and, in addition, is used as electron donor for a large variety of microbial metabolisms. Several types of bacteria and many non-methanogenic archaea can reduce sulfur. Microbial sulfur reduction was already shown in early studies, which highlighted the first proof of S0 reduction in a vibrioid bacterium from mud, with sulfur as electron acceptor and H
2 as electron donor. The first pure cultured species of sulfur-reducing bacteria, Desulfuromonas acetoxidans, was discovered in 1976 and described by Pfennig Norbert and Biebel Hanno as an anaerobic sulfur-reducing and acetate-oxidizing bacterium, not able to reduce sulfate. Only few taxa are true sulfur-reducing bacteria, using sulfur reduction as the only or main catabolic reaction. Normally, they couple this reaction with the oxidation of acetate, succinate or other organic compounds. In general, sulfate-reducing bacteria are able to use both sulfate and elemental sulfur as electron acceptors. Thanks to its abundancy and thermodynamic stability, sulfate is the most studied electron acceptor for anaerobic respiration that involves sulfur compounds. Elemental sulfur, however, is very abundant and important, especially in deep-sea hydrothermal vents, hot springs and other extreme environments, making its isolation more difficult. Some bacteria – such as Proteus, Campylobacter, Pseudomonas and Salmonella – have the ability to reduce sulfur, but can also use oxygen and other terminal electron acceptors.
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.
Lithotrophs are a diverse group of organisms using an inorganic substrate to obtain reducing equivalents for use in biosynthesis or energy conservation via aerobic or anaerobic respiration. While lithotrophs in the broader sense include photolithotrophs like plants, chemolithotrophs are exclusively microorganisms; no known macrofauna possesses the ability to use inorganic compounds as electron sources. Macrofauna and lithotrophs can form symbiotic relationships, in which case the lithotrophs are called "prokaryotic symbionts". An example of this is chemolithotrophic bacteria in giant tube worms or plastids, which are organelles within plant cells that may have evolved from photolithotrophic cyanobacteria-like organisms. Chemolithotrophs belong to the domains Bacteria and Archaea. The term "lithotroph" was created from the Greek terms 'lithos' (rock) and 'troph' (consumer), meaning "eaters of rock". Many but not all lithoautotrophs are extremophiles.
Beggiatoa is a genus of Gammaproteobacteria belonging to the order Thiotrichales, in the Pseudomonadota phylum. This genus was one of the first bacteria discovered by Ukrainian botanist Sergei Winogradsky. During his research in Anton de Bary's laboratory of botany in 1887, he found that Beggiatoa oxidized hydrogen sulfide (H2S) as an energy source, forming intracellular sulfur droplets, with oxygen as the terminal electron acceptor and CO2 used as a carbon source. Winogradsky named it in honor of the Italian doctor and botanist Francesco Secondo Beggiato (1806 - 1883), from Venice. Winogradsky referred to this form of metabolism as "inorgoxidation" (oxidation of inorganic compounds), today called chemolithotrophy. These organisms live in sulfur-rich environments such as soil, both marine and freshwater, in the deep sea hydrothermal vents and in polluted marine environments. The finding represented the first discovery of lithotrophy. Two species of Beggiatoa have been formally described: the type species Beggiatoa alba and Beggiatoa leptomitoformis, the latter of which was only published in 2017. This colorless and filamentous bacterium, sometimes in association with other sulfur bacteria (for example the genus Thiothrix), can be arranged in biofilm visible to the naked eye formed by a very long white filamentous mat, the white color is due to the stored sulfur. Species of Beggiatoa have cells up to 200 µm in diameter and they are one of the largest prokaryotes on Earth.
Gammaproteobacteria is a class of bacteria in the phylum Pseudomonadota. It contains about 250 genera, which makes it the most genus-rich taxon of the Prokaryotes. Several medically, ecologically, and scientifically important groups of bacteria belong to this class. It is composed by all Gram-negative microbes and is the most phylogenetically and physiologically diverse class of Proteobacteria.
Biomining is the technique of extracting metals from ores and other solid materials typically using prokaryotes, fungi or plants. These organisms secrete different organic compounds that chelate metals from the environment and bring it back to the cell where they are typically used to coordinate electrons. It was discovered in the mid 1900s that microorganisms use metals in the cell. Some microbes can use stable metals such as iron, copper, zinc, and gold as well as unstable atoms such as uranium and thorium. Large chemostats of microbes can be grown to leach metals from their media. These vats of culture can then be transformed into many marketable metal compounds. Biomining is an environmentally friendly technique compared to typical mining. Mining releases many pollutants while the only chemicals released from biomining is any metabolites or gasses that the bacteria secrete. The same concept can be used for bioremediation models. Bacteria can be inoculated into environments contaminated with metals, oils, or other toxic compounds. The bacteria can clean the environment by absorbing these toxic compounds to create energy in the cell. Bacteria can mine for metals, clean oil spills, purify gold, and use radioactive elements for energy.
Hydrogen-oxidizing bacteria are a group of facultative autotrophs that can use hydrogen as an electron donor. They can be divided into aerobes and anaerobes. The former use hydrogen as an electron donor and oxygen as an acceptor while the latter use sulphate or nitrogen dioxide as electron acceptors. Species of both types have been isolated from a variety of environments, including fresh waters, sediments, soils, activated sludge, hot springs, hydrothermal vents and percolating water.
Mariprofundus ferrooxydans is a neutrophilic, chemolithotrophic, Gram-negative bacterium which can grow by oxidising ferrous to ferric iron. It is one of the few members of the class Zetaproteobacteria in the phylum Pseudomonadota. It is typically found in iron-rich deep sea environments, particularly at hydrothermal vents. M. ferrooxydans characteristically produces stalks of solid iron oxyhydroxides that form into iron mats. Genes that have been proposed to catalyze Fe(II) oxidation in M. ferrooxydans are similar to those involved in known metal redox pathways, and thus it serves as a good candidate for a model iron oxidizing organism.
Sulfurimonas is a bacterial genus within the class of Campylobacterota, known for reducing nitrate, oxidizing both sulfur and hydrogen, and containing Group IV hydrogenases. This genus consists of four species: Sulfurimonas autorophica, Sulfurimonas denitrificans, Sulfurimonas gotlandica, and Sulfurimonas paralvinellae. The genus' name is derived from "sulfur" in Latin and "monas" from Greek, together meaning a “sulfur-oxidizing rod”. The size of the bacteria varies between about 1.5-2.5 μm in length and 0.5-1.0 μm in width. Members of the genus Sulfurimonas are found in a variety of different environments which include deep sea-vents, marine sediments, and terrestrial habitats. Their ability to survive in extreme conditions is attributed to multiple copies of one enzyme. Phylogenetic analysis suggests that members of the genus Sulfurimonas have limited dispersal ability and its speciation was affected by geographical isolation rather than hydrothermal composition. Deep ocean currents affect the dispersal of Sulfurimonas spp., influencing its speciation. As shown in the MLSA report of deep-sea hydrothermal vents Campylobacterota, Sulfurimonas has a higher dispersal capability compared with deep sea hydrothermal vent thermophiles, indicating allopatric speciation.
Katrina Jane Edwards was a pioneering geomicrobiologist known for her studies of organisms living below the ocean floor, specifically exploring the interactions between the microbes and their geological surroundings, and how global processes were influenced by these interactions. She spearheaded the Center for Dark Energy Biosphere Investigation (C-DEBI) project at the University of Southern California, which is ongoing. Edwards also helped organize the deep biosphere research community by heading the Fe-Oxidizing Microbial Observatory Project on Loihi Seamount, and serving on several program steering committees involving ocean drilling. Edwards taught at the Woods Hole Oceanographic Institution (WHOI) and later became a professor at the University of Southern California.[1][2]
Microbial oxidation of sulfur is the oxidation of sulfur by microorganisms to build their structural components. The oxidation of inorganic compounds is the strategy primarily used by chemolithotrophic microorganisms to obtain energy to survive, grow and reproduce. Some inorganic forms of reduced sulfur, mainly sulfide (H2S/HS−) and elemental sulfur (S0), can be oxidized by chemolithotrophic sulfur-oxidizing prokaryotes, usually coupled to the reduction of oxygen (O2) or nitrate (NO3−). Anaerobic sulfur oxidizers include photolithoautotrophs that obtain their energy from sunlight, hydrogen from sulfide, and carbon from carbon dioxide (CO2).
The hydrothermal vent microbial community includes all unicellular organisms that live and reproduce in a chemically distinct area around hydrothermal vents. These include organisms in the microbial mat, free floating cells, or bacteria in an endosymbiotic relationship with animals. Chemolithoautotrophic bacteria derive nutrients and energy from the geological activity at Hydrothermal vents to fix carbon into organic forms. Viruses are also a part of the hydrothermal vent microbial community and their influence on the microbial ecology in these ecosystems is a burgeoning field of research.
Vailuluʻu is a volcanic seamount discovered in 1975. It rises from the sea floor to a depth of 593 m (1,946 ft) and is located between Taʻu and Rose islands at the eastern end of the Samoa hotspot chain. The basaltic seamount is considered to mark the current location of the Samoa hotspot. The summit of Vailuluʻu contains a 2 km wide, 400 m deep oval-shaped caldera. Two principal rift zones extend east and west from the summit, parallel to the trend of the Samoan hotspot. A third less prominent rift extends southeast of the summit.
Eifuku and NW Eifuku (北西永福) are two seamounts in the Pacific Ocean. The better known one is NW Eifuku, where an unusual hydrothermal vent called "Champagne" produced droplets of liquid CO
2. Both seamounts are located in the Northern Marianas and are volcanoes, part of the Izu-Bonin-Mariana Arc. NW Eifuku rises to 1,535 metres (5,036 ft) depth below sea level and is a 9 kilometres (5.6 mi) wide volcanic cone.