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Anaerobic organism

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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.

First recorded observation

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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

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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:

  • Obligate anaerobes, which are harmed by the presence of oxygen.[5][6] Two examples of obligate anaerobes are Clostridium botulinum and the bacteria which live near hydrothermal vents on the deep-sea ocean floor.
  • Aerotolerant organisms, which cannot use oxygen for growth, but tolerate its presence.[7]
  • Facultative anaerobes, which can grow without oxygen but use oxygen if it is present.[7]

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

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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

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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

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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

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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

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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

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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

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

References

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  2. ^ Levinson, W. (2010). Review of Medical Microbiology and Immunology (11th ed.). McGraw-Hill. pp. 91–93. ISBN 978-0-07-174268-9.
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  4. ^ a b 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.
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  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.
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  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)
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  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. ^ a b 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. ^ a b 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. ^ a b 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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