Anaerobic organism

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Spinoloricus cinziae, a metazoan that metabolises with hydrogen, lacking mitochondria and instead using hydrogenosomes. Spinoloricus.png
Spinoloricus cinziae , a metazoan that metabolises with hydrogen, lacking mitochondria and instead using hydrogenosomes.

An anaerobic organism or anaerobe is any organism that does not require molecular oxygen for growth. It may react negatively or even die if free oxygen is present. In contrast, an aerobic organism (aerobe) is an organism that requires an oxygenated environment. Anaerobes may be unicellular (e.g. protozoans, [1] bacteria [2] ) or multicellular. [3] Most fungi are obligate aerobes, requiring oxygen to survive. However, some species, such as the Chytridiomycota that reside in the rumen of cattle, are obligate anaerobes; for these species, anaerobic respiration is used because oxygen will disrupt their metabolism or kill them. The sea floor is possibly one of the largest accumulation of anaerobic organisms on Earth, where microbes are primarily concentrated around hydrothermal vents. These microbes produce energy in absence of sunlight or oxygen through a process called chemosynthesis, whereby inorganic compounds such as hydrogen gas, hydrogen sulfide or ferrous ions are converted into organic matter.

Contents

First recorded observation

In his 14 June 1680 letter to The Royal Society, Antonie van Leeuwenhoek described an experiment he carried out by filling two identical glass tubes about halfway with crushed pepper powder, to which some clean rain water was added. Van Leeuwenhoek sealed one of the glass tubes using a flame and left the other glass tube open. Several days later, he discovered in the open glass tube 'a great many very little animalcules, of divers sort having its own particular motion.' Not expecting to see any life in the sealed glass tube, Van Leeuwenhoek saw to his surprise 'a kind of living animalcules that were round and bigger than the biggest sort that I have said were in the other water.' The conditions in the sealed tube had become quite anaerobic due to consumption of oxygen by aerobic microorganisms. [4]

In 1913, Martinus Beijerinck repeated Van Leeuwenhoek's experiment and identified Clostridium butyricum as a prominent anaerobic bacterium in the sealed pepper infusion tube liquid. Beijerinck commented:

We thus come to the remarkable conclusion that, beyond doubt, Van Leeuwenhoek in his experiment with the fully closed tube had cultivated and seen genuine anaerobic bacteria, which would happen again only after 200 years, namely about 1862 by Pasteur. That Leeuwenhoek, one hundred years before the discovery of oxygen and the composition of air, was not aware of the meaning of his observations is understandable. But the fact that in the closed tube he observed an increased gas pressure caused by fermentative bacteria and in addition saw the bacteria, prove in any case that he not only was a good observer, but also was able to design an experiment from which a conclusion could be drawn. [4]

Classifications

Aerobic and anaerobic bacteria can be differentiated by culturing them in test tubes of thioglycollate broth: Obligate aerobes need oxygen because they cannot ferment or respire anaerobically. They gather at the top of the tube where the oxygen concentration is highest. Obligate anaerobes are poisoned by oxygen, so they gather at the bottom of the tube where the oxygen concentration is lowest. Facultative anaerobes can grow with or without oxygen because they can metabolize energy aerobically or anaerobically. They gather mostly at the top because aerobic respiration generates more adenosine triphosphate (ATP) than either fermentation or anaerobic respiration. Microaerophiles need oxygen because they cannot ferment or respire anaerobically. However, they are poisoned by high concentrations of oxygen. They gather in the upper part of the test tube but not the very top. Aerotolerant organisms do not require oxygen as they metabolize energy anaerobically. Unlike obligate anaerobes, however, they are not poisoned by oxygen. They can/will be evenly distributed throughout the test tube. Ana.png
Aerobic and anaerobic bacteria can be differentiated by culturing them in test tubes of thioglycollate broth:
  1. Obligate aerobes need oxygen because they cannot ferment or respire anaerobically. They gather at the top of the tube where the oxygen concentration is highest.
  2. Obligate anaerobes are poisoned by oxygen, so they gather at the bottom of the tube where the oxygen concentration is lowest.
  3. Facultative anaerobes can grow with or without oxygen because they can metabolize energy aerobically or anaerobically. They gather mostly at the top because aerobic respiration generates more adenosine triphosphate (ATP) than either fermentation or anaerobic respiration.
  4. Microaerophiles need oxygen because they cannot ferment or respire anaerobically. However, they are poisoned by high concentrations of oxygen. They gather in the upper part of the test tube but not the very top.
  5. Aerotolerant organisms do not require oxygen as they metabolize energy anaerobically. Unlike obligate anaerobes, however, they are not poisoned by oxygen. They can/will be evenly distributed throughout the test tube.

For practical purposes, there are three categories of anaerobe:

However, this classification has been questioned after recent research showed that human "obligate anaerobes" (such as Finegoldia magna or the methanogenic archaea Methanobrevibacter smithii ) can be grown in aerobic atmosphere if the culture medium is supplemented with antioxidants such as ascorbic acid, glutathione and uric acid. [8] [9] [10] [11]

Energy metabolism

Some obligate anaerobes use fermentation, while others use anaerobic respiration. [12] Aerotolerant organisms are strictly fermentative. [13] In the presence of oxygen, facultative anaerobes use aerobic respiration. [7] In the absence of oxygen, some facultative anaerobes use fermentation, while others may use anaerobic respiration. [7]

Fermentation

There are many anaerobic fermentative reactions.

Fermentative anaerobic organisms typically use the lactic acid fermentation pathway:

C6H12O6 + 2 ADP + 2 phosphate → 2 lactic acid + 2 ATP + 2 H2O

The energy released in this reaction (without ADP and phosphate) is approximately 150 kJ per mol, which is conserved in generating two ATP from ADP per glucose. This is only 5% of the energy per sugar molecule that the typical aerobic reaction generates.

Plants and fungi (e.g., yeasts) in general use alcohol (ethanol) fermentation when oxygen becomes limiting:

C6H12O6 (glucose) + 2 ADP + 2 phosphate → 2 C2H5OH + 2 CO2↑ + 2 ATP + 2 H2O

The energy released is about 180 kJ per mol, which is conserved in generating two ATP from ADP per glucose.

Anaerobic bacteria and archaea use these and many other fermentative pathways, e.g., propionic acid fermentation, [14] butyric acid fermentation, [15] solvent fermentation, mixed acid fermentation, butanediol fermentation, Stickland fermentation, acetogenesis, or methanogenesis.[ citation needed ]

CrP hydrolysis

Creatine, an organic compound found in animals, provides a way for ATP to be utilized in the muscle. The phosphorylation of creatine allows for the storage of readily available phosphate that can be supplied to the muscles. [16]

creatine + ATP ⇌ phosphocreatine + ADP + H+

The reaction is reversible as well, allowing cellular ATP levels to be maintained during anoxic conditions. [17] This process in animals is seen to be coupled with metabolic suppression to allow certain fish, such as goldfish, to survive environmental anoxic conditions for a short period. [18]

Culturing anaerobes

Example of a workup algorithm of possible bacterial infection in cases with no specifically requested targets (non-bacteria, mycobacteria etc.), with most common situations and agents seen in a New England community hospital setting. Multiple anaerobic growth media are mentioned among agar plate cultures. Anaerobes may also be identified by MALDI-TOF as shown at bottom right. Diagnostic algorithm of possible bacterial infection.png
Example of a workup algorithm of possible bacterial infection in cases with no specifically requested targets (non-bacteria, mycobacteria etc.), with most common situations and agents seen in a New England community hospital setting. Multiple anaerobic growth media are mentioned among agar plate cultures. Anaerobes may also be identified by MALDI-TOF as shown at bottom right.

Since normal microbial culturing occurs in atmospheric air, which contains molecular oxygen, culturing of anaerobes requires special techniques. A number of techniques are employed by microbiologists when culturing anaerobic organisms, for example, handling the bacteria in a glovebox filled with nitrogen or the use of other specially sealed containers, or techniques such as injection of the bacteria into a dicot plant, which is an environment with limited oxygen. The GasPak System is an isolated container that achieves an anaerobic environment by the reaction of water with sodium borohydride and sodium bicarbonate tablets to produce hydrogen gas and carbon dioxide. Hydrogen then reacts with oxygen gas on a palladium catalyst to produce more water, thereby removing oxygen gas. The issue with the GasPak method is that an adverse reaction can take place where the bacteria may die, which is why a thioglycollate medium should be used. The thioglycollate supplies a medium mimicking that of a dicot plant, thus providing not only an anaerobic environment but all the nutrients needed for the bacteria to multiply. [19]

Recently, a French team evidenced a link between redox and gut anaerobes [20] based on clinical studies of severe acute malnutrition. [21] [note 1] These findings led to the development of aerobic culture of "anaerobes" by the addition of antioxidants in the culture medium. [22]

Multicellularity

Few multicellular life forms are anaerobic, since only aerobic respiration can provide enough energy for a complex metabolism. Exceptions include three species of Loricifera (< 1 mm in size) and the 10-cell Henneguya zschokkei . [23]

In 2010 three species of anaerobic loricifera were discovered in the hypersaline anoxic L'Atalante basin at the bottom of the Mediterranean Sea. They lack mitochondria which contain the oxidative phosphorylation pathway, which in all other animals combines oxygen with glucose to produce metabolic energy, and thus they consume no oxygen. Instead, these loricifera derive their energy from hydrogen, using hydrogenosomes. [24] [3]

Henneguya zschokkei also lack mitochondria, mitochondrial DNA, and oxidative pathways. The microscopic, parasitic cnidarian is observed to have mitochondria-related organelles contained within it. This mitochondria-related organelle within it is observed to have genes encoding for metabolic functions such as amino acid metabolism. However, these mitochondria-related organelles lack the key features of typical mitochondria found in closely related aerobic Myxobolus squamalus. Due to the difficulty of culturing H. zschokkei, there is little understanding of its anaerobic pathway. [25]

Symbiosis

Anaerobic respiration and its end products can facilitate symbiosis between anaerobes and aerobes. This occurs across taxa, often in compensation for nutritional needs. [26]

Anaerobiosis and symbiosis are found in interactions between ciliates and prokaryotes. Anaerobic ciliates interact with prokaryotes in an endosymbiotic relationship. These relationships are mediated in which the ciliate leaves end products that its prokaryotic symbiont utilizes. The ciliate achieves this through the use of fermentative metabolism. The rumen of various animals house this ciliate alongside many other anaerobic bacteria, protozoans, and fungi. [27] In specific, methanogenic archaea found in the rumen acts as a symbiont to anaerobic ciliates. [28] These anaerobes are useful to those with a rumen due to their ability to break down cellulose, making it bioavailable when otherwise indigestible by animals. [26]

Termites utilize anaerobic bacteria to fix and recapture nitrogen. In specific, the hindgut of the termite is full of nitrogen-fixing bacteria, ranging in function depending on the nitrogen concentration of the diet. Acetylene reduction in termites was observed to upregulate in termites with nitrogen-poor diets, meaning that nitrogenase activity rose as the nitrogen content of the termite was reduced. [29] One of the functions of termite microbiota is to recapture nitrogen from the termite's uric acid. This allows the conservation of nitrogen from an otherwise nitrogen-poor diet. [29] [30] The hindgut microbiome of different termites has been analyzed, showing 16 different anaerobic species of bacteria, including Clostridia, Enterobacteriaceae, and Gram-positive cocci. [30]

Notes

  1. ↑ This study was later retracted over ethical oversight concerns.

Related Research Articles

<span class="mw-page-title-main">Obligate aerobe</span> Organism that requires oxygen to grow

An obligate aerobe is an organism that requires oxygen to grow. Through cellular respiration, these organisms use oxygen to metabolise substances, like sugars or fats, to obtain energy. In this type of respiration, oxygen serves as the terminal electron acceptor for the electron transport chain. Aerobic respiration has the advantage of yielding more energy than fermentation or anaerobic respiration, but obligate aerobes are subject to high levels of oxidative stress.

<span class="mw-page-title-main">Aerobic organism</span> Organism that thrives in an oxygenated environment

An aerobic organism or aerobe is an organism that can survive and grow in an oxygenated environment. The ability to exhibit aerobic respiration may yield benefits to the aerobic organism, as aerobic respiration yields more energy than anaerobic respiration. Energy production of the cell involves the synthesis of ATP by an enzyme called ATP synthase. In aerobic respiration, ATP synthase is coupled with an electron transport chain in which oxygen acts as a terminal electron acceptor. In July 2020, marine biologists reported that aerobic microorganisms (mainly), in "quasi-suspended animation", were found in organically poor sediments, up to 101.5 million years old, 250 feet below the seafloor in the South Pacific Gyre (SPG), and could be the longest-living life forms ever found.

<span class="mw-page-title-main">Cellular respiration</span> Process to convert glucose to ATP in cells

Cellular respiration is the process by which biological fuels are oxidized in the presence of an inorganic electron acceptor, such as oxygen, to drive the bulk production of adenosine triphosphate (ATP), which contains energy. Cellular respiration may be described as a set of metabolic reactions and processes that take place in the cells of organisms to convert chemical energy from nutrients into ATP, and then release waste products.

<span class="mw-page-title-main">Lactic acid fermentation</span> Series of interconnected biochemical reactions

Lactic acid fermentation is a metabolic process by which glucose or other six-carbon sugars are converted into cellular energy and the metabolite lactate, which is lactic acid in solution. It is an anaerobic fermentation reaction that occurs in some bacteria and animal cells, such as muscle cells.

A mesophile is an organism that grows best in moderate temperature, neither too hot nor too cold, with an optimum growth range from 20 to 45 °C. The optimum growth temperature for these organisms is 37 °C. The term is mainly applied to microorganisms. Organisms that prefer extreme environments are known as extremophiles. Mesophiles have diverse classifications, belonging to two domains: Bacteria, Archaea, and to kingdom Fungi of domain Eucarya. Mesophiles belonging to the domain Bacteria can either be gram-positive or gram-negative. Oxygen requirements for mesophiles can be aerobic or anaerobic. There are three basic shapes of mesophiles: coccus, bacillus, and spiral.

Anaerobic respiration is respiration using electron acceptors other than molecular oxygen (O2). Although oxygen is not the final electron acceptor, the process still uses a respiratory electron transport chain.

<span class="mw-page-title-main">Facultative anaerobic organism</span> Beings that can respire with and without oxygen

A facultative anaerobic organism is an organism that makes ATP by aerobic respiration if oxygen is present, but is capable of switching to fermentation if oxygen is absent.

<span class="mw-page-title-main">Obligate anaerobe</span> Microorganism killed by normal atmospheric levels of oxygen

Obligate anaerobes are microorganisms killed by normal atmospheric concentrations of oxygen (20.95% O2). Oxygen tolerance varies between species, with some species capable of surviving in up to 8% oxygen, while others lose viability in environments with an oxygen concentration greater than 0.5%.

Diazotrophs are bacteria and archaea that fix atmospheric nitrogen (N2) in the atmosphere into bioavailable forms such as ammonia.

<span class="mw-page-title-main">Microaerophile</span> Microorganism requiring lower levels of oxygen than normally found in atmosphere

A microaerophile is a microorganism that requires environments containing lower levels of dioxygen than that are present in the atmosphere (i.e. < 21% O2; typically 2–10% O2) for optimal growth. A more restrictive interpretation requires the microorganism to be obligate in this requirement. Many microaerophiles are also capnophiles, requiring an elevated concentration of carbon dioxide (e.g. 10% CO2 in the case of Campylobacter species).

<span class="mw-page-title-main">Sulfur-reducing bacteria</span> Microorganisms able to reduce elemental sulfur to hydrogen sulfide

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.

<span class="mw-page-title-main">Capnophile</span> Microorganism that flourishes in a carbon dioxide rich environment

Capnophiles are microorganisms that thrive in the presence of high concentrations of carbon dioxide.

<i>Rhodospirillum rubrum</i> Species of bacterium

Rhodospirillum rubrum is a Gram-negative, pink-coloured bacterium, with a size of 800 to 1000 nanometers. It is a facultative anaerobe, thus capable of using oxygen for aerobic respiration under aerobic conditions, or an alternative terminal electron acceptor for anaerobic respiration under anaerobic conditions. Alternative terminal electron acceptors for R. rubrum include dimethyl sulfoxide or trimethylamine oxide.

Microbial metabolism is the means by which a microbe obtains the energy and nutrients it needs to live and reproduce. Microbes use many different types of metabolic strategies and species can often be differentiated from each other based on metabolic characteristics. The specific metabolic properties of a microbe are the major factors in determining that microbe's ecological niche, and often allow for that microbe to be useful in industrial processes or responsible for biogeochemical cycles.

In biology, syntrophy, syntrophism, or cross-feeding is the cooperative interaction between at least two microbial species to degrade a single substrate. This type of biological interaction typically involves the transfer of one or more metabolic intermediates between two or more metabolically diverse microbial species living in close proximity to each other. Thus, syntrophy can be considered an obligatory interdependency and a mutualistic metabolism between different microbial species, wherein the growth of one partner depends on the nutrients, growth factors, or substrates provided by the other(s).

The Pasteur effect describes how available oxygen inhibits ethanol fermentation, driving yeast to switch toward aerobic respiration for increased generation of the energy carrier adenosine triphosphate (ATP). More generally, in the medical literature, the Pasteur effect refers to how the cellular presence of oxygen causes in cells a decrease in the rate of glycolysis and also a suppression of lactate accumulation. The effect occurs in animal tissues, as well as in microorganisms belonging to the fungal kingdom.

Aerobic denitrification, or co-respiration, the simultaneous use of both oxygen (O2) and nitrate (NO−3) as oxidizing agents, performed by various genera of microorganisms. This process differs from anaerobic denitrification not only in its insensitivity to the presence of oxygen, but also in its higher potential to form nitrous oxide (N2O) as a byproduct.

The Arc system is a two-component system found in some bacteria that regulates gene expression in faculatative anaerobes such as Escheria coli. Two-component system means that it has a sensor molecule and a response regulator. Arc is an abbreviation for Anoxic Redox Control system. Arc systems are instrumental in maintaining energy metabolism during transcription of bacteria. The ArcA response regulator looks at growth conditions and expresses genes to best suit the bacteria. The Arc B sensor kinase, which is a tripartite protein, is membrane bound and can autophosphorylate.

Robert Edward Hungate was a pioneering American microbial ecologist who developed the first techniques for the culturing of anaerobic microbes in his study of the bovine rumen.

Columbia Nalidixic Acid (CNA) agar is a growth medium used for the isolation and cultivation of bacteria from clinical and non-clinical specimens. CNA agar contains antibiotics that inhibit Gram-negative organisms, aiding in the selective isolation of Gram-positive bacteria. Gram-positive organisms that grow on the media can be differentiated on the basis of hemolysis.

References

  1. ↑ Upcroft P, Upcroft JA (January 2001). "Drug Targets and Mechanisms of Resistance in". Clin. Microbiol. Rev. 14 (1): 150–164. doi:10.1128/CMR.14.1.150-164.2001. PMC   88967 . PMID   11148007.
  2. ↑ Levinson, W. (2010). Review of Medical Microbiology and Immunology (11th ed.). McGraw-Hill. pp. 91–93. ISBN   978-0-07-174268-9.
  3. 1 2 Danovaro R; Dell'anno A; Pusceddu A; Gambi C; et al. (April 2010). "The first metazoa living in permanently anoxic conditions". BMC Biology. 8 (1): 30. doi: 10.1186/1741-7007-8-30 . PMC   2907586 . PMID   20370908.
  4. 1 2 Gest, Howard. (2004) The discovery of microorganisms by Robert Hooke and Antoni van Leeuwenhoek, Fellows of the Royal Society, in: 'The Royal Society May 2004 Volume: 58 Issue: 2: pp. 12.
  5. ↑ Prescott LM, Harley JP, Klein DA (1996). Microbiology (3rd ed.). Wm. C. Brown Publishers. pp. 130–131. ISBN   978-0-697-29390-9.
  6. ↑ Brooks GF, Carroll KC, Butel JS, Morse SA (2007). Jawetz, Melnick & Adelberg's Medical Microbiology (24th ed.). McGraw Hill. pp. 307–312. ISBN   978-0-07-128735-7.
  7. 1 2 3 4 Hogg, S. (2005). Essential Microbiology (1st ed.). Wiley. pp. 99–100. ISBN   978-0-471-49754-7.
  8. ↑ La Scola, B.; Khelaifia, S.; Lagier, J.-C.; Raoult, D. (2014). "Aerobic culture of anaerobic bacteria using antioxidants: a preliminary report". European Journal of Clinical Microbiology & Infectious Diseases. 33 (10): 1781–1783. doi:10.1007/s10096-014-2137-4. ISSN   0934-9723. PMID   24820294. S2CID   16682688.
  9. ↑ Dione, N.; Khelaifia, S.; La Scola, B.; Lagier, J.C.; Raoult, D. (2016). "A quasi-universal medium to break the aerobic/anaerobic bacterial culture dichotomy in clinical microbiology". Clinical Microbiology and Infection. 22 (1): 53–58. doi: 10.1016/j.cmi.2015.10.032 . PMID   26577141.
  10. ↑ Khelaifia, S.; Lagier, J.-C.; Nkamga, V. D.; Guilhot, E.; Drancourt, M.; Raoult, D. (2016). "Aerobic culture of methanogenic archaea without an external source of hydrogen". European Journal of Clinical Microbiology & Infectious Diseases. 35 (6): 985–991. doi:10.1007/s10096-016-2627-7. ISSN   0934-9723. PMID   27010812. S2CID   17258102.
  11. ↑ Traore, S.I.; Khelaifia, S.; Armstrong, N.; Lagier, J.C.; Raoult, D. (2019). "Isolation and culture of Methanobrevibacter smithii by co-culture with hydrogen-producing bacteria on agar plates". Clinical Microbiology and Infection. 25 (12): 1561.e1–1561.e5. doi: 10.1016/j.cmi.2019.04.008 . PMID   30986553.
  12. ↑ Pommerville, Jeffrey (2010). Alcamo's Fundamentals of Microbiology. Jones and Bartlett Publishers. p. 177. ISBN   9781449655822.
  13. ↑ Slonim, Anthony; Pollack, Murray (2006). Pediatric Critical Care Medicine. Lippincott Williams & Wilkins. p. 130. ISBN   9780781794695.
  14. ↑ Piwowarek, Kamil; Lipińska, Edyta; Hać-Szymańczuk, Elżbieta; Kieliszek, Marek; Ścibisz, Iwona (January 2018). "Propionibacterium spp.—source of propionic acid, vitamin B12, and other metabolites important for the industry". Applied Microbiology and Biotechnology. 102 (2): 515–538. doi:10.1007/s00253-017-8616-7. ISSN   0175-7598. PMC   5756557 . PMID   29167919.
  15. ↑ Seedorf, Henning; Fricke, W. Florian; Veith, Birgit; Brüggemann, Holger; Liesegang, Heiko; Strittmatter, Axel; Miethke, Marcus; Buckel, Wolfgang; Hinderberger, Julia; Li, Fuli; Hagemeier, Christoph; Thauer, Rudolf K.; Gottschalk, Gerhard (2008-02-12). "The genome of Clostridium kluyveri , a strict anaerobe with unique metabolic features". Proceedings of the National Academy of Sciences. 105 (6): 2128–2133. Bibcode:2008PNAS..105.2128S. doi: 10.1073/pnas.0711093105 . ISSN   0027-8424. PMC   2542871 . PMID   18218779.
  16. ↑ Sahlin, Kent; Harris, Roger C. (2011-05-01). "The creatine kinase reaction: a simple reaction with functional complexity". Amino Acids. 40 (5): 1363–1367. doi:10.1007/s00726-011-0856-8. ISSN   1438-2199. PMID   21394603. S2CID   12877062.
  17. ↑ Wang, Y.; Richards, J. G. (2011-01-01), "HYPOXIA | Anaerobic Metabolism in Fish", in Farrell, Anthony P. (ed.), Encyclopedia of Fish Physiology, San Diego: Academic Press, pp. 1757–1763, doi:10.1016/b978-0-12-374553-8.00154-4, ISBN   978-0-08-092323-9 , retrieved 2023-04-18
  18. ↑ van den Thillart, G.; van Waarde, A.; Muller, H. J.; Erkelens, C.; Addink, A.; Lugtenburg, J. (1989-04-01). "Fish muscle energy metabolism measured by in vivo 31P-NMR during anoxia and recovery". American Journal of Physiology. Regulatory, Integrative and Comparative Physiology. 256 (4): R922–R929. doi:10.1152/ajpregu.1989.256.4.R922. ISSN   0363-6119. PMID   2705580.
  19. ↑ "GasPak System" Archived 2009-09-28 at the Wayback Machine . Accessed May 3, 2008.
  20. ↑ Million, Matthieu; Raoult, Didier (December 2018). "Linking gut redox to human microbiome". Human Microbiome Journal. 10: 27–32. doi: 10.1016/j.humic.2018.07.002 .
  21. ↑ Million, Matthieu; Tidjani Alou, Maryam; Khelaifia, Saber; Bachar, Dipankar; Lagier, Jean-Christophe; Dione, Niokhor; Brah, Souleymane; Hugon, Perrine; Lombard, Vincent; Armougom, Fabrice; Fromonot, Julien (May 2016). "Increased Gut Redox and Depletion of Anaerobic and Methanogenic Prokaryotes in Severe Acute Malnutrition". Scientific Reports. 6 (1): 26051. Bibcode:2016NatSR...626051M. doi:10.1038/srep26051. ISSN   2045-2322. PMC   4869025 . PMID   27183876. (Retracted, see doi:10.1038/s41598-023-44597-3, PMID   37903811)
  22. ↑ Guilhot, Elodie; Khelaifia, Saber; La Scola, Bernard; Raoult, Didier; Dubourg, Grégory (March 2018). "Methods for culturing anaerobes from human specimen". Future Microbiology. 13 (3): 369–381. doi:10.2217/fmb-2017-0170. ISSN   1746-0913. PMID   29446650.
  23. ↑ Scientists discovered the first animal that doesn't need oxygen to live
  24. ↑ Oxygen-Free Animals Discovered-A First, National Geographic news
  25. ↑ Yahalomi, Dayana; Atkinson, Stephen D.; Neuhof, Moran; Chang, E. Sally; Philippe, Hervé; Cartwright, Paulyn; Bartholomew, Jerri L.; Huchon, Dorothée (2020-03-10). "A cnidarian parasite of salmon (Myxozoa: Henneguya ) lacks a mitochondrial genome". Proceedings of the National Academy of Sciences. 117 (10): 5358–5363. Bibcode:2020PNAS..117.5358Y. doi: 10.1073/pnas.1909907117 . ISSN   0027-8424. PMC   7071853 . PMID   32094163.
  26. 1 2 Moran, Nancy A. (2006-10-24). "Symbiosis". Current Biology. 16 (20): R866–R871. doi: 10.1016/j.cub.2006.09.019 . ISSN   0960-9822. PMID   17055966. S2CID   235311996.
  27. ↑ Flint, Harry J. (September 1994). "Molecular genetics of obligate anaerobes from the rumen". FEMS Microbiology Letters. 121 (3): 259–267. doi: 10.1111/j.1574-6968.1994.tb07110.x . ISSN   0378-1097. PMID   7926679. S2CID   24273083.
  28. ↑ Rotterová, Johana; Edgcomb, Virginia P.; Čepička, Ivan; Beinart, Roxanne (September 2022). "Anaerobic ciliates as a model group for studying symbioses in oxygen‐depleted environments". Journal of Eukaryotic Microbiology. 69 (5): e12912. doi:10.1111/jeu.12912. ISSN   1066-5234. PMID   35325496. S2CID   247677842.
  29. 1 2 Breznak, John A.; Brill, Winston J.; Mertins, James W.; Coppel, Harry C. (August 1973). "Nitrogen Fixation in Termites". Nature. 244 (5418): 577–580. Bibcode:1973Natur.244..577B. doi:10.1038/244577a0. ISSN   1476-4687. PMID   4582514. S2CID   4223979.
  30. 1 2 Thong-On, Arunee; Suzuki, Katsuyuki; Noda, Satoko; Inoue, Jun-ichi; Kajiwara, Susumu; Ohkuma, Moriya (2012). "Isolation and Characterization of Anaerobic Bacteria for Symbiotic Recycling of Uric Acid Nitrogen in the Gut of Various Termites". Microbes and Environments. 27 (2): 186–192. doi:10.1264/jsme2.ME11325. PMC   4036019 . PMID   22791052.
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