Cyanobacteria

Cyanobacteria /sˌænbækˈtɪəriə/, also known as Cyanophyta, are a phylum of prokaryotes consisting of both free-living photosynthetic bacteria and the endosymbiotic plastids that are present in the Archaeplastida, the autotrophic eukaryotes that include the red and green algae and land plants. They commonly obtain their energy through oxygenic photosynthesis,[4] which produces the oxygen gas in the atmosphere of Earth.[5] The name cyanobacteria comes from their color (Greek: κυανός, romanized: kyanós, lit. 'blue'),[6][7] giving them their other name, "blue-green algae",[4][8] though some modern botanists restrict the term algae to eukaryotes.[9] They appear to have originated in freshwater or a terrestrial environment.[10]

Cyanobacteria
Temporal range: 2100–0 Ma
Microscope image of Cylindrospermum, a filamentous genus of cyanobacteria
Scientific classification
Domain: Bacteria
(unranked): Terrabacteria
(unranked): Cyanobacteria-Melainabacteria group
Phylum: Cyanobacteria
Stanier, 1973
Class: Cyanophyceae
Orders[1]

As of 2014 the taxonomy was under revision[2][3]

Synonyms
  • Myxophyceae Wallroth, 1833
  • Phycochromaceae Rabenhorst, 1865
  • Cyanophyceae Sachs, 1874
  • Schizophyceae Cohn, 1879
  • Cyanophyta Steinecke, 1931
  • Oxyphotobacteria Gibbons & Murray, 1978
Light microscope view of cyanobacteria from a microbial mat

Unlike heterotrophic prokaryotes, cyanobacteria have internal membranes. These are flattened sacs called thylakoids where photosynthesis is performed.[11][12]

Phototrophic eukaryotes such as green plants perform photosynthesis in plastids that are thought to have their ancestry in cyanobacteria, acquired long ago via a process called endosymbiosis. These endosymbiotic cyanobacteria in eukaryotes then evolved and differentiated into specialized organelles such as chloroplasts, etioplasts and leucoplasts.

By producing and releasing oxygen (as a byproduct of photosynthesis), cyanobacteria are thought to have converted the early oxygen-poor, reducing atmosphere into an oxidizing one, causing the Great Oxygenation Event and the "rusting of the Earth",[13] which dramatically changed the composition of the Earth's life forms and led to the near-extinction of anaerobic organisms.[14]

Cyanobacteria produce a range of toxins known as cyanotoxins that can pose a danger to humans and animals.

The cyanobacteria Synechocystis and Cyanothece are important model organisms with potential applications in biotechnology for bioethanol production, food colorings, as a source of human and animal food, dietary supplements and raw materials.

Description

Cyanobacteria are a group of photosynthetic bacteria, some of which are nitrogen-fixing, that live in a wide variety of moist soils and water either freely or in a symbiotic relationship with plants or lichen-forming fungi (as in the lichen genus Peltigera).[15] They range from unicellular to filamentous and include colonial species. Colonies may form filaments, sheets, or even hollow spheres. Some filamentous species can differentiate into several different cell types: vegetative cells – the normal, photosynthetic cells that are formed under favorable growing conditions; akinetes – climate-resistant spores that may form when environmental conditions become harsh; and thick-walled heterocysts – which contain the enzyme nitrogenase, vital for nitrogen fixation[16][17][18] in an anaerobic environment due to its sensitivity to oxygen.[18]

Nitrogen fixation

Some cyanobacteria can fix atmospheric nitrogen in anaerobic conditions by means of specialized cells called heterocysts.[17][18] Heterocysts may also form under the appropriate environmental conditions (anoxic) when fixed nitrogen is scarce. Heterocyst-forming species are specialized for nitrogen fixation and are able to fix nitrogen gas into ammonia (NH
3
), nitrites (NO
2
) or nitrates (NO
3
), which can be absorbed by plants and converted to protein and nucleic acids (atmospheric nitrogen is not bioavailable to plants, except for those having endosymbiotic nitrogen-fixing bacteria, especially the family Fabaceae, among others).

Free-living cyanobacteria are present in the water of rice paddies, and cyanobacteria can be found growing as epiphytes on the surfaces of the green alga, Chara, where they may fix nitrogen.[19] Cyanobacteria such as Anabaena (a symbiont of the aquatic fern Azolla) can provide rice plantations with biofertilizer.[20]

Morphology

Colonies of Nostoc pruniforme

Many cyanobacteria form motile filaments of cells, called hormogonia, that travel away from the main biomass to bud and form new colonies elsewhere.[21][22] The cells in a hormogonium are often thinner than in the vegetative state, and the cells on either end of the motile chain may be tapered. To break away from the parent colony, a hormogonium often must tear apart a weaker cell in a filament, called a necridium.

Each individual cell (each single cyanobacterium) typically has a thick, gelatinous cell wall.[23] They lack flagella, but hormogonia of some species can move about by gliding along surfaces.[24] Many of the multicellular filamentous forms of Oscillatoria are capable of a waving motion; the filament oscillates back and forth. In water columns, some cyanobacteria float by forming gas vesicles, as in archaea.[25] These vesicles are not organelles as such. They are not bounded by lipid membranes but by a protein sheath.

Ecology

Cyanobacteria can be found in almost every terrestrial and aquatic habitat oceans, fresh water, damp soil, temporarily moistened rocks in deserts, bare rock and soil, and even Antarctic rocks. They can occur as planktonic cells or form phototrophic biofilms. They are found in endolithic ecosystem.[26] A few are endosymbionts in lichens, plants, various protists, or sponges and provide energy for the host. Some live in the fur of sloths, providing a form of camouflage.[27]

Aquatic cyanobacteria are known for their extensive and highly visible blooms that can form in both freshwater and marine environments. The blooms can have the appearance of blue-green paint or scum. These blooms can be toxic, and frequently lead to the closure of recreational waters when spotted. Marine bacteriophages are significant parasites of unicellular marine cyanobacteria.[28]

Environmental impact of cyanobacteria and other photosynthetic microorganisms in aquatic systems. Different classes of photosynthetic microorganisms are found in aquatic and marine environments where they form the base of healthy food webs and participate in symbioses with other organisms. However, shifting environmental conditions can result in community dysbiosis, where the growth of opportunistic species can lead to harmful blooms and toxin production with negative consequences to human health, livestock and fish stocks. Positive interactions are indicated by arrows; negative interactions are indicated by closed circles on the ecological model.[29]

Cyanobacterial growth is favored in ponds and lakes where waters are calm and have little turbulent mixing.[30] Their life cycles are disrupted when the water naturally or artificially mixes from churning currents caused by the flowing water of streams or the churning water of fountains. For this reason blooms of cyanobacteria seldom occur in rivers unless the water is flowing slowly. Growth is also favored at higher temperatures which enable Microcystis species to outcompete diatoms and green algae, and potentially allow development of toxins.[30]

Based on environmental trends, models and observations suggest cyanobacteria will likely increase their dominance in aquatic environments. This can lead to serious consequences, particularly the contamination of sources of drinking water. Cyanobacteria can interfere with water treatment in various ways, primarily by plugging filters (often large beds of sand and similar media) and by producing cyanotoxins, which have the potential to cause serious illness if consumed. Consequences may also lie within fisheries and waste management practices. Anthropogenic eutrophication, rising temperatures, vertical stratification and increased atmospheric carbon dioxide are contributors to cyanobacteria increasing dominance of aquatic ecosystems.[31]

Cyanobacteria have been found to play an important role in terrestrial habitats. It has been widely reported that cyanobacteria soil crusts help to stabilize soil to prevent erosion and retain water.[32] An example of a cyanobacterial species that does so is Microcoleus vaginatus. M. vaginatus stabilizes soil using a polysaccharide sheath that binds to sand particles and absorbs water.[33]

Some of these organisms contribute significantly to global ecology and the oxygen cycle. The tiny marine cyanobacterium Prochlorococcus was discovered in 1986 and accounts for more than half of the photosynthesis of the open ocean.[34] Circadian rhythms were once thought to only exist in eukaryotic cells but many cyanobacteria display a bacterial circadian rhythm.

"Cyanobacteria are arguably the most successful group of microorganisms on earth. They are the most genetically diverse; they occupy a broad range of habitats across all latitudes, widespread in freshwater, marine, and terrestrial ecosystems, and they are found in the most extreme niches such as hot springs, salt works, and hypersaline bays. Photoautotrophic, oxygen-producing cyanobacteria created the conditions in the planet's early atmosphere that directed the evolution of aerobic metabolism and eukaryotic photosynthesis. Cyanobacteria fulfill vital ecological functions in the world's oceans, being important contributors to global carbon and nitrogen budgets." – Stewart and Falconer[35]

Photosynthesis

Cyanobacteria have several unique features. As the endosymbiotic plastids are endosymbiotic cyanobacteria, they share these features insofar as they have not lost them.

Carbon fixation

Cyanobacteria use the energy of sunlight to drive photosynthesis, a process where the energy of light is used to synthesize organic compounds from carbon dioxide. Because they are aquatic organisms, they typically employ several strategies which are collectively known as a "carbon concentrating mechanism" to aid in the acquisition of inorganic carbon (CO
2
or bicarbonate). Among the more specific strategies is the widespread prevalence of the bacterial microcompartments known as carboxysomes.[36] These icosahedral structures are composed of hexameric shell proteins that assemble into cage-like structures that can be several hundreds of nanometers in diameter. It is believed that these structures tether the CO
2
-fixing enzyme, RuBisCO, to the interior of the shell, as well as the enzyme carbonic anhydrase, using metabolic channeling to enhance the local CO
2
concentrations and thus increase the efficiency of the RuBisCO enzyme.[37]

Electron transport

In contrast to purple bacteria and other bacteria performing anoxygenic photosynthesis, thylakoid membranes of cyanobacteria are not continuous with the plasma membrane but are separate compartments.[38] The photosynthetic machinery is embedded in the thylakoid membranes, with phycobilisomes acting as light-harvesting antennae attached to the membrane, giving the green pigmentation observed (with wavelengths from 450 nm to 660 nm) in most cyanobacteria.[39]

Diagram of a typical cyanobacterial cell

While most of the high-energy electrons derived from water are used by the cyanobacterial cells for their own needs, a fraction of these electrons may be donated to the external environment via electrogenic activity.[40]

Respiration

Respiration in cyanobacteria can occur in the thylakoid membrane alongside photosynthesis,[41] with their photosynthetic electron transport sharing the same compartment as the components of respiratory electron transport. While the goal of photosynthesis is to store energy by building carbohydrates from CO2, respiration is the reverse of this, with carbohydrates turned back into CO2 accompanying energy release.

Cyanobacteria appear to separate these two processes with their plasma membrane containing only components of the respiratory chain, while the thylakoid membrane hosts an interlinked respiratory and photosynthetic electron transport chain.[41] Cyanobacteria use electrons from succinate dehydrogenase rather than from NADPH for respiration.[41]

Cyanobacteria only respire during the night (or in the dark) because the facilities used for electron transport are used in reverse for photosynthesis while in the light.[42]

Electron transport chain

Many cyanobacteria are able to reduce nitrogen and carbon dioxide under aerobic conditions, a fact that may be responsible for their evolutionary and ecological success. The water-oxidizing photosynthesis is accomplished by coupling the activity of photosystem (PS) II and I (Z-scheme). In contrast to green sulfur bacteria which only use one photosystem, the use of water as an electron donor is energetically demanding, requiring two photosystems.[43]

Attached to the thylakoid membrane, phycobilisomes act as light-harvesting antennae for the photosystems.[44] The phycobilisome components (phycobiliproteins) are responsible for the blue-green pigmentation of most cyanobacteria.[45] The variations on this theme are due mainly to carotenoids and phycoerythrins that give the cells their red-brownish coloration. In some cyanobacteria, the color of light influences the composition of the phycobilisomes.[46][47] In green light, the cells accumulate more phycoerythrin, whereas in red light they produce more phycocyanin. Thus, the bacteria appear green in red light and red in green light.[48] This process of complementary chromatic adaptation is a way for the cells to maximize the use of available light for photosynthesis.

A few genera lack phycobilisomes and have chlorophyll b instead (Prochloron, Prochlorococcus, Prochlorothrix). These were originally grouped together as the prochlorophytes or chloroxybacteria, but appear to have developed in several different lines of cyanobacteria. For this reason, they are now considered as part of the cyanobacterial group.[49][50]

Metabolism

In general, photosynthesis in cyanobacteria uses water as an electron donor and produces oxygen as a byproduct, though some may also use hydrogen sulfide[51] a process which occurs among other photosynthetic bacteria such as the purple sulfur bacteria.

Carbon dioxide is reduced to form carbohydrates via the Calvin cycle.[52] The large amounts of oxygen in the atmosphere are considered to have been first created by the activities of ancient cyanobacteria.[53] They are often found as symbionts with a number of other groups of organisms such as fungi (lichens), corals, pteridophytes (Azolla), angiosperms (Gunnera), etc.[54]

There are some groups capable of heterotrophic growth,[55] while others are parasitic, causing diseases in invertebrates or algae (e.g., the black band disease).[56][57][58]

Relationship to chloroplasts

Primary chloroplasts are cell organelles found in some eukaryotic lineages, where they are specialized in performing photosynthesis. They are considered to have evolved from endosymbiotic cyanobacteria.[59][60] After some years of debate,[61] it is now generally accepted that the three major groups of primary endosymbiotic eukaryotes (i.e. green plants, red algae and glaucophytes) form one large monophyletic group called Archaeplastida, which evolved after one unique endosymbiotic event.[62][63][64][65]

The morphological similarity between chloroplasts and cyanobacteria was first reported by German botanist Andreas Franz Wilhelm Schimper in the 19th century[66] Chloroplasts are only found in plants and algae,[67] thus paving the way for Russian biologist Konstantin Mereschkowski to suggest the symbiogenic origin of the plastid in 1905.[68] Lynn Margulis brought this hypothesis back to attention more than 60 years later[69] but the idea did not become fully accepted until supplementary data started to accumulate. The cyanobacterial origin of plastids is now supported by various pieces of phylogenetic,[70][62][65] genomic,[71] biochemical[72][73] and structural evidence.[74] The description of another independent and more recent primary endosymbiosis event between a cyanobacterium and a separate eukaryote lineage (the rhizarian Paulinella chromatophora) also gives credibility to the endosymbiotic origin of the plastids.[75]

In addition to this primary endosymbiosis, many eukaryotic lineages have been subject to secondary or even tertiary endosymbiotic events, that is the "Matryoshka-like" engulfment by a eukaryote of another plastid-bearing eukaryote.[76][59]

Within this evolutionary context, it is noteworthy that, as far as we can tell, oxygenic photosynthesis only evolved once (in prokaryotic cyanobacteria), and all photosynthetic eukaryotes (including all plants and algae) have acquired this ability from them. In other words, all the oxygen that makes the atmosphere breathable for aerobic organisms originally comes from cyanobacteria or their later descendants.[77]

DNA repair

Cyanobacteria are challenged by environmental stresses and internally generated reactive oxygen species that cause DNA damage. Cyanobacteria possess numerous E. coli-like DNA repair genes.[78] Several DNA repair genes are highly conserved in cyanobacteria, even in small genomes, suggesting that core DNA repair processes such as recombinational repair, nucleotide excision repair and methyl-directed DNA mismatch repair are common among cyanobacteria.[78]

Natural genetic transformation

Cyanobacteria are capable of natural genetic transformation.[79][80][81] Natural genetic transformation is the genetic alteration of a cell resulting from the direct uptake and incorporation of exogenous DNA from its surroundings. For bacterial transformation to take place, the recipient bacteria must be in a state of competence, which may occur in nature as a response to conditions such as starvation, high cell density or exposure to DNA damaging agents. In chromosomal transformation, homologous transforming DNA can be integrated into the recipient genome by homologous recombination, and this process appears to be an adaptation for repairing DNA damage.[82]

Classification

Tree of Life in Generelle Morphologie der Organismen (1866). Note the location of the genus Nostoc with algae and not with bacteria (kingdom "Monera")

Historically, bacteria were first classified as plants constituting the class Schizomycetes, which along with the Schizophyceae (blue-green algae/Cyanobacteria) formed the phylum Schizophyta,[83] then in the phylum Monera in the kingdom Protista by Haeckel in 1866, comprising Protogens, Protamaeba, Vampyrella, Protomonae, and Vibrio, but not Nostoc and other cyanobacteria, which were classified with algae,[84] later reclassified as the Prokaryotes by Chatton.[85]

The cyanobacteria were traditionally classified by morphology into five sections, referred to by the numerals I–V. The first three – Chroococcales, Pleurocapsales, and Oscillatoriales – are not supported by phylogenetic studies. The latter two – Nostocales and Stigonematales – are monophyletic, and make up the heterocystous cyanobacteria.[86][87]

The members of Chroococales are unicellular and usually aggregate in colonies. The classic taxonomic criterion has been the cell morphology and the plane of cell division. In Pleurocapsales, the cells have the ability to form internal spores (baeocytes). The rest of the sections include filamentous species. In Oscillatoriales, the cells are uniseriately arranged and do not form specialized cells (akinetes and heterocysts).[88] In Nostocales and Stigonematales, the cells have the ability to develop heterocysts in certain conditions. Stigonematales, unlike Nostocales, include species with truly branched trichomes.[86]

Most taxa included in the phylum or division Cyanobacteria have not yet been validly published under The International Code of Nomenclature of Prokaryotes (ICNP) except:

The remainder are validly published under the International Code of Nomenclature for algae, fungi, and plants.

Formerly, some bacteria, like Beggiatoa, were thought to be colorless Cyanobacteria.[89]

Earth history

Stromatolites are layered biochemical accretionary structures formed in shallow water by the trapping, binding, and cementation of sedimentary grains by biofilms (microbial mats) of microorganisms, especially cyanobacteria.[90]

Stromatolites left behind by cyanobacteria are the oldest known fossils of life on Earth. This one-billion-year-old fossil is from Glacier National Park in Montana.

During the Precambrian, stromatolite communities of microorganisms grew in most marine and non-marine environments in the photic zone. After the Cambrian explosion of marine animals, grazing on the stromatolite mats by herbivores greatly reduced the occurrence of the stromatolites in marine environments. Since then, they are found mostly in hypersaline conditions where grazing invertebrates cannot live (e.g. Shark Bay, Western Australia). Stromatolites provide ancient records of life on Earth by fossil remains which date from 3.5 Ga ago.[91] As of 2010 the oldest undisputed evidence of cyanobacteria is from 2.1 Ga ago, but there is some evidence for them as far back as 2.7 Ga ago. Oxygen concentrations in the atmosphere remained around or below 1% of today's level until 2.4 Ga ago (the Great Oxygenation Event). The rise in oxygen may have caused a fall in the concentration of atmospheric methane, and triggered the Huronian glaciation from around 2.4 to 2.1 Ga ago. In this way, cyanobacteria may have killed off much of the other bacteria of the time.[92]

Oncolites are sedimentary structures composed of oncoids, which are layered structures formed by cyanobacterial growth. Oncolites are similar to stromatolites, but instead of forming columns, they form approximately spherical structures that were not attached to the underlying substrate as they formed.[93] The oncoids often form around a central nucleus, such as a shell fragment,[94] and a calcium carbonate structure is deposited by encrusting microbes. Oncolites are indicators of warm waters in the photic zone, but are also known in contemporary freshwater environments.[95] These structures rarely exceed 10 cm in diameter.

One former classification scheme of cyanobacterial fossils divided them into the porostromata and the spongiostromata. These are now recognized as form taxa and considered taxonomically obsolete; however, some authors have advocated for the terms remaining informally to describe form and structure of bacterial fossils.[96]

Biotechnology and applications

The unicellular cyanobacterium Synechocystis sp. PCC6803 was the third prokaryote and first photosynthetic organism whose genome was completely sequenced.[97] It continues to be an important model organism.[98] Cyanothece ATCC 51142 is an important diazotrophic model organism. The smallest genomes have been found in Prochlorococcus spp. (1.7 Mb)[99][100] and the largest in Nostoc punctiforme (9 Mb).[101] Those of Calothrix spp. are estimated at 12–15 Mb,[102] as large as yeast.

Recent research has suggested the potential application of cyanobacteria to the generation of renewable energy by directly converting sunlight into electricity. Internal photosynthetic pathways can be coupled to chemical mediators that transfer electrons to external electrodes.[103] In the shorter term, efforts are underway to commercialize algae-based fuels such as diesel, gasoline, and jet fuel.[40][104][105]

Cyanobacteria cultured in specific media: Cyanobacteria can be helpful in agriculture as they have the ability to fix atmospheric nitrogen in soil.

Researchers from a company called Algenol have cultured genetically modified cyanobacteria in sea water inside a clear plastic enclosure so they first make sugar (pyruvate) from CO
2
and the water via photosynthesis. Then, the bacteria secrete ethanol from the cell into the salt water. As the day progresses, and the solar radiation intensifies, ethanol concentrations build up and the ethanol itself evaporates onto the roof of the enclosure. As the sun recedes, evaporated ethanol and water condense into droplets, which run along the plastic walls and into ethanol collectors, from where it is extracted from the enclosure with the water and ethanol separated outside the enclosure. As of March 2013, Algenol was claiming to have tested its technology in Florida and to have achieved yields of 9,000 US gallons per acre per year.[106] This could potentially meet US demands for ethanol in gasoline in 2025, assuming a B30 blend, from an area of around half the size of California's San Bernardino County, requiring less than one-tenth of the area than ethanol from other biomass, such as corn, and only very limited amounts of fresh water.[107]

Cyanobacteria may possess the ability to produce substances that could one day serve as anti-inflammatory agents and combat bacterial infections in humans.[108]

Spirulina's extracted blue color is used as a natural food coloring in gum and candy.[109]

Possible use off-Earth, e.g. Mars

Researchers from several space agencies argue that cyanobacteria could be used for producing goods for human consumption in future manned outposts on Mars, by transforming materials available on this planet.[110]

Health risks

Some cyanobacteria can produce neurotoxins, cytotoxins, endotoxins, and hepatotoxins (e.g., the microcystin-producing bacteria genus microcystis), which are collectively known as cyanotoxins.

Specific toxins include, anatoxin-a, guanitoxin, aplysiatoxin, cyanopeptolin, cylindrospermopsin, domoic acid, nodularin R (from Nodularia), neosaxitoxin, and saxitoxin. Cyanobacteria reproduce explosively under certain conditions. This results in algal blooms, which can become harmful to other species, and pose a danger to humans and animals, if the cyanobacteria involved produce toxins. Several cases of human poisoning have been documented, but a lack of knowledge prevents an accurate assessment of the risks.[111][112][113]

Recent studies suggest that significant exposure to high levels of cyanobacteria producing toxins such as BMAA can cause amyotrophic lateral sclerosis (ALS). People living within half a mile of cyanobacterially contaminated lakes have had a 2.3 times greater risk of developing ALS than the rest of the population; people around New Hampshire's Lake Mascoma had an up to 25 times greater risk of ALS than the expected incidence.[114] BMAA from desert crusts found throughout Qatar might have contributed to higher rates of ALS in Gulf War veterans.[112][115]

Chemical control

Several chemicals can eliminate cyanobacterial blooms from smaller water-based systems such as swimming pools. They include: calcium hypochlorite, copper sulphate, cupricide, and simazine.[116] The calcium hypochlorite amount needed varies depending on the cyanobacteria bloom, and treatment is needed periodically. According to the Department of Agriculture Australia, a rate of 12 g of 70% material in 1000 l of water is often effective to treat a bloom.[116] Copper sulfate is also used commonly, but no longer recommended by the Australian Department of Agriculture, as it kills livestock, crustaceans, and fish.[116] Cupricide is a chelated copper product that eliminates blooms with lower toxicity risks than copper sulfate. Dosage recommendations vary from 190 ml to 4.8 l per 1000 m2.[116] Ferric alum treatments at the rate of 50 mg/l will reduce algae blooms.[116][117] Simazine, which is also a herbicide, will continue to kill blooms for several days after an application. Simazine is marketed at different strengths (25, 50, and 90%), the recommended amount needed for one cubic meter of water per product is 25% product 8 ml; 50% product 4 ml; or 90% product 2.2 ml.[116]

Dietary supplementation

Spirulina tablets

Some cyanobacteria are sold as food, notably Aphanizomenon flos-aquae and Arthrospira platensis (Spirulina).[118]

Despite the associated toxins which many members of this phylum produce, some microalgae also contain substances of high biological value, such as polyunsaturated fatty acids, amino acids, proteins, pigments, antioxidants, vitamins, and minerals.[119] Edible blue-green algae reduce the production of pro-inflammatory cytokines by inhibiting NF-κB pathway in macrophages and splenocytes.[120] Sulfate polysaccharides exhibit immunomodulatory, antitumor, antithrombotic, anticoagulant, anti-mutagenic, anti-inflammatory, antimicrobial, and even antiviral activity against HIV, herpes, and hepatitis.[121]

See also

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