Methanobrevibacter smithii

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Phase-contrast photo of Methanobrevibacter smithii PS M. smithii.jpg
Phase-contrast photo of Methanobrevibacter smithii PS

Methanobrevibacter smithii
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Archaea
Kingdom: Euryarchaeota
Class: Methanobacteria
Order: Methanobacteriales
Family: Methanobacteriaceae
Genus: Methanobrevibacter
Species:
M. smithii
Binomial name
Methanobrevibacter smithii
Balch and Wolfe 1981

Methanobrevibacter smithii is the predominant methanogenic archaeon in the microbiota of the human gut. [1] M. smithii has a coccobacillus shape. It plays an important role in the efficient digestion of polysaccharides (complex sugars) by consuming the end products of bacterial fermentation (H2, CO2, acetate, and formate). [2] M. smithii is a hydrogenotrophic methanogen that utilizes hydrogen by combining it with carbon dioxide to form methane. The removal of hydrogen by M. smithii is thought to allow an increase in the extraction of energy from nutrients by shifting bacterial fermentation to more oxidized end products. [3]

Contents

Importance in the human gut

Methanobrevibacter smithii is an anaerobic archaea which enjoys colonizing the colon and rectum thanks to its anaerobic environment, optimal pH (6.5-7), and slow transit time. [4] [5] M. smithii is the most common methanogenic archaeon in the human gut microbiota. M. smithii is paramount in digestive processes, and has a high prevalence in human feces. [6] M. smithii is found in breast milk and breast feeding is a major route of M. smithii acquisition and colonization in newborns. [4] Methanogens, including M. smithii, play a role as one of the three central hydrogen-consuming microorganisms or hydrogenotrophs in the human gut microbiota, along with various acetogenic bacteria and sulfate-reducing bacteria. Understanding these microorganisms and how they contribute to hydrogen metabolism in the gut can provide insight into the efficiency of dietary fermentation. [7] Accumulation of hydrogen in the gut reduces the efficiency of microbial fermentation. [8] Methanogenic archaea are therefore particularly significant for the human gut, because they are pivotal in the removal of excess hydrogen. [3]

Metabolism

M. smithii presents a relatively greater expression of genes which employ carbon dioxide (CO2), hydrogen gas (H2), and formate (HCO−2) for methanogenesis, compared to non-gut methanogens. [9] The main energy producing route of M. smithii metabolism comes from the utilization of hydrogen and carbon dioxide shown in the equation: 4H2+CO2 → CH4+ 2H2O. [4] M. smithii can also use formate as a carbon source by converting it to CO2 via formate dehydrogenase ezymes. [9] [10] It also has an intact pathway to allow for CO2 utilization gene cluster for the methanogenic consumption of Bacteroides thetaiotaomicron -produced metabolite. [9]

M. smithii supports methanogenic and nonmethanogenic removal of diverse bacterial end products of fermentation. [9]

The dominant archaeon in the human gut ecosystem affects the specificity and efficiency of bacterial digestion of dietary polysaccharides. This influences the person’s calorie harvest and body fat. [9] M. smithii, along with certain bacteria, is more often found in lean individuals than in those who are overweight. [11] Researchers have sequenced M. smithii genome, indicating that M. smithii may be a therapeutic target for reducing energy harvest in obese humans. [9]

Microbial interactions

Methanobrevibacter Smithii is able to interact with Bacteroides thetaiotaomicron in mouse co-colonization studies where they alter the metabolic pathways of each other. [9] In the presence of M. smithii,B.thetaiotaomicron increases its production of acetate which can be utilized by an incomplete reductive tricarboxylic acid cycle (rTCA) in M. smithii for biosynthesis. [9] During this relationship, M. smithii also increases expression of its metabolic pathways for nitrogen assimilation, ethanol and methanol utilization, and formate utilization. This relationship was found to significantly decrease the cecal ethanol content in co-colonized mice due the increased utilization by M. smithii. [9]

The gut microbiota is dominated by gram-negative Bacteroidota, and Bacillota (mostly gram-positive). Archaea are most prominently represented by the methanogenic M. smithii. M. smithii is believed to be a therapeutic target for manipulation and an adaptation to the gut ecosystem. [9]

M. smithii in human health and disease

In Anorexic Patients

In 2009, the largest human study concerning obesity and gut microbiota to date was conducted. Obesity disorders are the result of an imbalance and have serious consequences such as cardiovascular disease, type 2 diabetes, and colon cancer. The gut microbiota and environment contributes to the energy imbalance because of its involvement in energy intake, conversion and storage. Culture-independent methods have shown that high proportions of methanogens can comprise up to 10% of all anaerobes in the colons of healthy adults. The quantification average of M. smithii for the anorexic group was much greater than the lean and obese group. Thus, higher amounts of M. smithii were found in anorexic patients than lean patients.

The development of Methanobrevibacter in anorexia patients may be associated with an adaptive attempt towards optimal exploitation of the low caloric diet of anorexic patients. Hence, an increase in M. smithii leads to the optimization of food transformation in low caloric diets. M. smithii could also be related to constipation, a common condition for anorexic patients. [3]

M. smithii and constipation

Observational studies show a strong association between delayed intestinal transit and the production of methane. [12] Experimental data suggest a direct inhibitory activity of methane on the colonic and ileal smooth muscle and a possible role for methane as a gasotransmitter. Statins can inhibit archaeal cell membrane biosynthesis apparently without affecting bacterial numbers as demonstrated in livestock and humans. This opens the possibility of a therapeutic intervention that targets a specific etiological factor of constipation while protecting the intestinal microbiome. While it is generally believed that statins inhibit methane production via their effect on cell membrane biosynthesis, mediated by inhibition of the HMG-CoA reductase, there is accumulating evidence for an alternative or additional mechanism of action where statins inhibit methanogenesis directly. It appears that this other mechanism may predominate when the lactone form of statins, particularly lovastatin, is administered. [13]

Other Disease Associations

Methanobrevibacter smithii is also found in dental plaque and in the vagina (with vaginosis). [14]

Cell wall and cell membrane compared to bacteria

The cell wall and cell membrane of Methanobrevibacter smithii determine susceptibility to antibiotics and statins. The cell wall is composed of pseudopeptidoglycan (and not peptidoglycan as in bacteria) which makes archaea resistant to lysozyme and many antibiotics that interfere with cell wall synthesis. The cell membrane consists of a lipid bilayer or monolayer, the backbone of which is composed of isoprene units that are linked to glycerol by ether bonds. In contrast, the lipid bilayer of bacteria consists of a fatty acid backbone that is linked to glycerol by an ester bond. The presence of statin-sensitive isoprene units in the cell membrane of archaea allows statins to selectively interfere with the growth of archaea while leaving the cell membrane of bacteria unaffected. While bacteria do not use isoprene units in their cell membrane they are still required elsewhere. These bacterial isoprene units are, however, synthesized by the mevalonate pathway (MEP) that is not inhibited by statins. [13]

Viruses

Methanobrevibacter smithii PS chromosome contains a provirus derived from the integration of a head-tailed archaeal virus genome. [15] The provirus was shown to be sporadically induced, resulting in release of virions with isometric icoahedral capsids and long non-contractile tails (siphovirus-like morphology). [16] The Methanobrevibacter smithii tailed virus 1 (MSTV1) was found to coexists with its host in a stable equilibrium, with average virus-to-host ratio maintained at ~0.1 both in vitro and in vivo. A similar dynamics is also typical of bacteriophages infecting gut bacteria, suggesting that bacterial and archaeal viruses in the gastrointestinal tract have convergence of a similar propagation strategy. [16]

Related Research Articles

Methanogens are anaerobic archaea that produce methane as a byproduct of their energy metabolism, i.e., catabolism. Methane production, or methanogenesis, is the only biochemical pathway for ATP generation in methanogens. All known methanogens belong exclusively to the domain Archaea, although some bacteria, plants, and animal cells are also known to produce methane. However, the biochemical pathway for methane production in these organisms differs from that in methanogens and does not contribute to ATP formation. Methanogens belong to various phyla within the domain Archaea. Previous studies placed all known methanogens into the superphylum Euryarchaeota. However, recent phylogenomic data have led to their reclassification into several different phyla. Methanogens are common in various anoxic environments, such as marine and freshwater sediments, wetlands, the digestive tracts of animals, wastewater treatment plants, rice paddy soil, and landfills. While some methanogens are extremophiles, such as Methanopyrus kandleri, which grows between 84 and 110°C, or Methanonatronarchaeum thermophilum, which grows at a pH range of 8.2 to 10.2 and a Na+ concentration of 3 to 4.8 M, most of the isolates are mesophilic and grow around neutral pH.

Methanogenesis or biomethanation is the formation of methane coupled to energy conservation by microbes known as methanogens. It is the fourth and final stage of anaerobic digestion. Organisms capable of producing methane for energy conservation have been identified only from the domain Archaea, a group phylogenetically distinct from both eukaryotes and bacteria, although many live in close association with anaerobic bacteria. The production of methane is an important and widespread form of microbial metabolism. In anoxic environments, it is the final step in the decomposition of biomass. Methanogenesis is responsible for significant amounts of natural gas accumulations, the remainder being thermogenic.

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).

Methanocaldococcus formerly known as Methanococcus is a genus of coccoid methanogen archaea. They are all mesophiles, except the thermophilic M. thermolithotrophicus and the hyperthermophilic M. jannaschii. The latter was discovered at the base of a “white smoker” chimney at 21°N on the East Pacific Rise and it was the first archaean genome to be completely sequenced, revealing many novel and eukaryote-like elements.

<i>Methanobacterium</i> Genus of archaea

Methanobacterium is a genus of the Methanobacteria class in the Archaea kingdom, which produce methane as a metabolic byproduct. Despite the name, this genus belongs not to the bacterial domain but the archaeal domain. Methanobacterium are nonmotile and live without oxygen, which is toxic to them, and they only inhabit anoxic environments.

Methanosphaera is a genus of microbes within the family Methanobacteriaceae. It was distinguished from other genera within Methanobacteriaceae in 1985 on the basis of the oligonucleotide sequence of its 16S RNA. Like other archaea within Methanobacteriaceae, those of Methanosphaera are methanogens, but while most use formate to reduce carbon dioxide, those of Methanosphaera use hydrogen to reduce methanol to methane.

<span class="mw-page-title-main">Archaea</span> Domain of organisms

Archaea is a domain of organisms. Traditionally, Archaea only included its prokaryotic members, but this since has been found to be paraphyletic, as eukaryotes are now known to have evolved from archaea. Even though the domain Archaea includes eukaryotes, the term "archaea" in English still generally refers specifically to prokaryotic members of Archaea. Archaea were initially classified as bacteria, receiving the name archaebacteria, but this term has fallen out of use.

Archaeol is a diether composed of two phytanyl chains linked to the sn-2 and sn-3 positions of glycerol. As its phosphate ester, it is a common component of the membranes of archaea.

Methanocaldococcus jannaschii is a thermophilic methanogenic archaean in the class Methanococci. It was the first archaeon, and third organism, to have its complete genome sequenced. The sequencing identified many genes unique to the archaea. Many of the synthesis pathways for methanogenic cofactors were worked out biochemically in this organism, as were several other archaeal-specific metabolic pathways.

Methanobrevibacter cuticularis is a species of methanogen archaeon. It was first isolated from the hindgut of the termite Reticulitermes flavipes. It is rod-shaped, ranging in size from 0.34 to 1.6 μm and possesses polar fibers. Its morphology, gram-positive staining reaction, resistance to cell lysis by chemical agents and narrow range of utilizable substrates are typical of species belonging to the family Methanobacteriaceae. It habitates on or near the hindgut epithelium and also attached to filamentous prokaryotes associated with the gut wall. It is one of the predominant gut biota.

Methanobrevibacter curvatus is a species of methanogen archaeon. It was first isolated from the hindgut of the termite Reticulitermes flavipes. It is rod-shaped, ranging in size from 0.34 to 1.6 μm and possesses polar fibers. Its morphology, gram-positive staining reaction, resistance to cell lysis by chemical agents and narrow range of utilisable substrates are typical of species belonging to the family Methanobacteriaceae.

Methanobrevibacter filiformis is a species of methanogen archaeon. It was first isolated from the hindgut of the termite Reticulitermes flavipes. It is rod-shaped and possesses polar fibers. Its morphology, gram-positive staining reaction, resistance to cell lysis by chemical agents and narrow range of utilisable substrates are typical of species belonging to the family Methanobacteriaceae. It habitates on or near the hindgut epithelium and also attached to filamentous prokaryotes associated with the gut wall. It is one of the predominant gut biota.

Methanobrevibacter woesei is a species of methanogen archaeon, named after Carl R. Woese.

Methanococcoides burtonii is a methylotrophic methanogenic archaeon first isolated from Ace Lake, Antarctica. Its type strain is DSM 6242.

Methanosphaera stadtmanae is a methanogen archaeon. It is a non-motile, Gram-positive, spherical-shaped organism that obtains energy by using hydrogen to reduce methanol to methane. It does not possess cytochromes and is part of the large intestine's biota.

<i>Methanococcus maripaludis</i> Species of archaeon

Methanococcus maripaludis is a species of methanogenic archaea found in marine environments, predominantly salt marshes. M. maripaludis is a non-pathogenic, gram-negative, weakly motile, non-spore-forming, and strictly anaerobic mesophile. It is classified as a chemolithoautotroph. This archaeon has a pleomorphic coccoid-rod shape of 1.2 by 1.6 μm, in average size, and has many unique metabolic processes that aid in survival. M. maripaludis also has a sequenced genome consisting of around 1.7 Mbp with over 1,700 identified protein-coding genes. In ideal conditions, M. maripaludis grows quickly and can double every two hours.

Syntrophococcus sucromutans is a Gram-negative strictly anaerobic chemoorganotrophic Bacillota. These bacteria can be found forming small chains in the habitat where it was first isolated, the rumen of cows. It is the type strain of genus Syntrophococcus and it has an uncommon one-carbon metabolic pathway, forming acetate from formate as a product of sugar oxidation.

<i>Methanosarcina barkeri</i> Species of archaea

Methanosarcina barkeri is the type species of the genus Methanosarcina, characterized by its wide range of substrates used in methanogenesis. While most known methanogens produce methane from H2 and CO2, M. barkeri can also dismutate methylated compounds such as methanol or methylamines, oxidize acetate, and reduce methylated compounds with H2. This makes M. barkeri one of the few Methanosarcina species capable of utilizing all four known methanogenesis pathways. Even among other Methanosarcinales, which commonly utilize a broad range of substrates, the ability to grow on H2 and CO2 is rare due to the requirement for high H2 partial pressure. Like other Methanosarcina species, M. barkeri has a large genome (4.53 Mbp for the type strain MS, 4.9 Mbp for the Wiesmoor strain, and 4.5 Mbp for the CM2 strain), although it is significantly smaller than the largest archaeal genome of Methanosarcina acetivorans (5.75 Mbp for the type strain C2A). It is also one of the few archaea, particularly among anaerobic species, that is genetically tractable and can be used for genetic studies.

Methanobrevibacter oralis is a methanogenic archaeon species considered to be a member of the human microbiota, mainly associated to the oral cavity. M. oralis is a coccobacillary shaped, single-cell, Gram-positive, non-motile microorganism of the Archaea domain of life. This species has been isolated and sequenced from humans in dental plaque and in their gastrointestinal tract. As a methanogen and a hydrogenotroph, this prokaryote can produce methane by using hydrogen and carbon dioxide as substrates through a process called methanogenesis.

References

  1. ↑ Miller, Terry L.; Wolin, Meyer J. (February 1982). "Enumeration of Methanobrevibacter smithii in human feces". Archives of Microbiology. 131 (1): 14–18. doi:10.1007/BF00451492. ISSN   0302-8933.
  2. ↑ Whitman, William B., ed. (2015-09-14). Bergey's Manual of Systematics of Archaea and Bacteria (1 ed.). Wiley. doi:10.1002/9781118960608.gbm00496. ISBN   978-1-118-96060-8.
  3. 1 2 3 Armougom F; Henry M; Vialettes B; Raccah D; et al. (2009). "Monitoring Bacterial Community of Human Gut Microbiota Reveals an Increase in Lactobacillus in Obese Patients and Methanogens in Anorexic Patients". PLOS ONE. 4 (9): e7125. Bibcode:2009PLoSO...4.7125A. doi: 10.1371/journal.pone.0007125 . PMC   2742902 . PMID   19774074.
  4. 1 2 3 Malat, Ihab; Drancourt, Michel; Grine, Ghiles (September 2024). "Methanobrevibacter smithii cell variants in human physiology and pathology: A review". Heliyon. 10 (18): e36742. doi: 10.1016/j.heliyon.2024.e36742 . PMC   11437934 . PMID   39347381.
  5. ↑ McCallum, Giselle; Tropini, Carolina (2024). "The gut microbiota and its biogeography". Nature Reviews Microbiology. 22 (2): 105–118. doi:10.1038/s41579-023-00969-0. ISSN   1740-1534.
  6. ↑ Bedis, D., Mireille, H. (2009). "High Prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae Detected in the Human Gut Using an Improved DNA Detection Protocol." PLOS One 4(9) e7063.
  7. ↑ Hansen, Elizabeth E.; Lozupone, Catherine A.; Rey, Federico E.; Wu, Meng; Guruge, Janaki L.; Narra, Aneesha; Goodfellow, Jonathan; Zaneveld, Jesse R.; McDonald, Daniel T. (2011-03-15). "Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins". Proceedings of the National Academy of Sciences of the United States of America. 108 Suppl 1 (Suppl 1): 4599–4606. Bibcode:2011PNAS..108.4599H. doi: 10.1073/pnas.1000071108 . ISSN   1091-6490. PMC   3063581 . PMID   21317366.
  8. ↑ Smith, Nick W.; Shorten, Paul R.; Altermann, Eric H.; Roy, Nicole C.; McNabb, Warren C. (2019-05-04). "Hydrogen cross-feeders of the human gastrointestinal tract". Gut Microbes. 10 (3): 270–288. doi:10.1080/19490976.2018.1546522. ISSN   1949-0976. PMC   6546324 . PMID   30563420.
  9. 1 2 3 4 5 6 7 8 9 10 Buck, S., Hansen, E., (2007). "Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut." Proceedings of the National Academy of Sciences of the United States of America 104, 10643-10648.
  10. ↑ Lyu, Zhe; Shao, Nana; Akinyemi, Taiwo; Whitman, William B. (2018-07-09). "Methanogenesis". Current Biology. 28 (13): R727 –R732. doi:10.1016/j.cub.2018.05.021. ISSN   0960-9822.
  11. ↑ Stenman LK, Burcelin R, Lahtinen S (2016). "Establishing a causal link between gut microbes, body weight gain and glucose metabolism in humans - towards treatment with probiotics". Beneficial Microbes . 7 (1): 11–22. doi:10.3920/BM2015.0069. PMID   26565087.
  12. ↑ Sahakian, Ara B.; Jee, Sam-Ryong; Pimentel, Mark (2010-08-01). "Methane and the Gastrointestinal Tract". Digestive Diseases and Sciences. 55 (8): 2135–2143. doi:10.1007/s10620-009-1012-0. ISSN   1573-2568.
  13. 1 2 Gottlieb, K., Wacher, V., Sliman, J., & Pimentel, M. (2015). Review article: inhibition of methanogenic archaea by statins as a targeted management strategy for constipation and related disorders. Alimentary Pharmacology & Therapeutics.
  14. ↑ Belay, N; Mukhopadhyay, B; Conway de Macario, E; Galask, R; Daniels, L. 1990. Methanogenic bacteria in human vaginal samples. Journal of Clinical Microbiology, 28 (7), 1666–1668.
  15. ↑ Krupovic, M; Forterre, P; Bamford, DH (2010). "Comparative analysis of the mosaic genomes of tailed archaeal viruses and proviruses suggests common themes for virion architecture and assembly with tailed viruses of bacteria". Journal of Molecular Biology. 397 (1): 144–60. doi:10.1016/j.jmb.2010.01.037. PMID   20109464.
  16. 1 2 Baquero, DP; Medvedeva, S; Martin-Gallausiaux, C; Pende, N; Sartori-Rupp, A; Tachon, S; Pedron, T; Debarbieux, L; Borrel, G; Gribaldo, S; Krupovic, M (2024). "Stable coexistence between an archaeal virus and the dominant methanogen of the human gut". Nature Communications. 15 (1): 7702. doi:10.1038/s41467-024-51946-x. PMC   11375127 . PMID   39231967.

Further reading

Bang, Corinna; Weidenbach, Katrin; Gutsmann, Thomas; Heine, Holgar; Schmitz, Ruth A. (2014). "The Intestinal Archaea Methanosphaera stadtmanae and Methanobrevibacter smithii Activate Human Dendritic Cells". PLOS ONE. 9 (6): e99411. Bibcode:2014PLoSO...999411B. doi: 10.1371/journal.pone.0099411 . PMC   4051749 . PMID   24915454.

Kim, Gene; Deepinder, Fnu; Morales, Walter; Hwang, Laura; Weitsman, Stacy; Chang, Christopher; Gunsalus, Robert; Pimentel, Mark (December 2012). "Methanobrevibacter smithii Is the Predominant Methanogen in Patients with Constipation-Predominant IBS and Methane on Breath". Digestive Diseases and Sciences. 57 (12): 3213–3218. doi:10.1007/s10620-012-2197-1. PMID   22573345. S2CID   207113756.

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