Bacteroides thetaiotaomicron
Scientific classification Edit this classification
Domain: Bacteria
Phylum: Bacteroidota
Class: Bacteroidia
Order: Bacteroidales
Family: Bacteroidaceae
Genus: Bacteroides
Species:
B. thetaiotaomicron
Binomial name
Bacteroides thetaiotaomicron
(Distaso 1912) Castellani and Chalmers 1919

Bacteroides thetaiotaomicron is a gram-negative, rod shaped obligate anaerobic bacterium that is a prominent member of the normal gut microbiome in the distal intestines. Its proteome, consisting of 4,779 members, includes a system for obtaining and breaking down dietary polysaccharides that would otherwise be difficult to digest.[1] B. thetaiotaomicron is also an opportunistic pathogen, meaning it may become virulent in immunocompromised individuals. It is often used in research as a model organism for functional studies of the human microbiota.[2]

History and taxonomy

Bacteroides thetaiotaomicron was first described in 1912 under the name Bacillus thetaiotaomicron and moved to the genus Bacteroides in 1919.[3] The B. thetaiotaomicron type strain VPI-5482 was originally isolated from a healthy adult's human feces.[1] The specific name derives from the Greek letters theta, iota, and omicron; the List of Prokaryotic names with Standing in Nomenclature indicates this as "relating to the morphology of vacuolated forms".[3] The Bacteroidota bacterial phylum, distinguished by its unique motility, is present in a wide range of ecosystems, habitats, lifestyles, and physiological conditions.[4] The name is used as an example of an "arbitrary" species name in the International Code of Nomenclature of Prokaryotes.[5][6]

Genome

The genome of B. thetaiotaomicron was sequenced in 2003. It is one circular chromosome of double stranded DNA. It is 6.26 megabases in length, but has a relatively small number of distinct genes, due to genes coding for proteins that are unusually large compared to other prokaryotes.[1] This genomic feature is shared with another member of the genus, Bacteroides fragilis.[7] The genome contains genes associated with breaking down polysaccharides, including glycoside hydrolases and starch binding proteins.[1][7] These genes along with ECF-type sigma factors allow B. thetaiotaomicron to correlate the availability of nutrients with expression of the particular genes.[1] The genome also contains many genes encoding proteins involved in sensing and responding to the extracellular environment, such as sigma factors and two-component systems.[1][8][9] The colocalization of the gene encoding digestive enzymes with extracytoplasmic function sigma factors and signal transduction systems creates a mechanism that regulates gene expression based on the availability of nutrients in the environment.[1] The B. thetaiotaomicron genome encodes a large number of small non-coding RNAs which also play a key role in regulatory processes, though few have been characterized to date.[2] B. thetaiotaomicron has several different types of mobile genetic elements, including a 33 kilobase plasmid, 63 transposases, and four homologs of the conjugative transposon CTnDOT. CTnDOT encodes the resistance to the antibiotics erythromycin and tetracycline, and is horizontally transferred between Bacteroides species as well as other gut microbiota.[1]

Metabolism

Bacteroides thetaiotaomicron is capable of metabolizing a very diverse range of otherwise indigestible polysaccharides, like amylose, amylopectin, and pullulan.[8] Its complement of enzymes used for hydrolysis of glycosidic bonds is among the largest known in prokaryotes, and is even thought to be capable of hydrolyzing nearly all glycosidic bonds in biological polysaccharides. As the major organism of the human gut flora to break down plant polysaccharides it can use both dietary carbohydrates, as well as those sourced from the host, depending on nutrient availability.[10] Complex plant polysaccharides, unlike simple monosaccharides and disaccharides that are digested and absorbed in the small intestines, are left to be used as a food source in the colon.[11] B. thetaiotaomicron is able to dominate the many other gut bacteria living within the human colonic environment using its superior ability to acquire sufficient nutrients.[11] This is possible due to the combined effects of an increased amount of glycosyl hydrolases, that degrade enzymes, membrane binding proteins, and sugar-specific transporters.[11] There are 172 glycosylhydrolases produced by B. thetaiotaomicron which is greater than any other sequenced bacterium, contributing to enzymes that contribute products of hydrolysis to the host.[11] All Bacteriodes employ polysaccharide-utilization loci (PULs) whose gene clusters encode systems that target and degrade carbohydrates.[12] Apart of these systems are carbohydrate-active enzymes (CAZymes) that can very efficiently degrade complex carbohydrates found in the diet. There have been three different PULs identified that use RG-II, a dietary carbohydrate with the most structural complexity, as a substrate The RG-II degradome contains 23 enzymes that target sequential glycosidic linkage in the RG-II, leading to its disassembly.[12]

B. thetaiotaomicron is aerotolerant and can survive, but not grow, when exposed to oxygen. Oxygen has limited access in eukaryotic host environments, like the human intestines. Generation of reactive oxygen species (ROS) such as hydrogen peroxide may occur, threatening the flora by attacking iron cofactors enzymes widely used in metabolism.[13] To drive the oxygen concentration to lower levels, B. thetaiotaomicron expresses a number of proteins that scavenge ROS such as hydrogen peroxide when exposed to air.[13]

Role in the human microbiome

Members of the genus Bacteroides accounts for about a quarter of the microbial population in an adult human's intestine. In a long-term study of Bacteroides species in clinical samples, B. thetaiotaomicron was the second most common species isolated, behind Bacteroides fragilis.[13] It is crucial to humans as it is able to digest plant materials that enzymes within the gut cannot.[1]

B. thetaiotaomicron is considered commensal, a type of symbiosis, meaning it provides the host with key benefits like digestion.[1][7] B. thetaiotaomicron has far more glycosyl hydrolases, in which 61% are located in the outer membrane or extracellular matrix, suggesting that the digestive capabilities serve the bacteria's host more than anything.[8] The glycosyl hydrolases express 23 specific enzymatic functions that supply the host or even other microbes in the gut flora with the breakdown products of hydrolysis.[11] The polysaccharides that are digested by B. thetaiotaomicron are converted into monosaccharides which can then be absorbed by human cells for metabolism.[11]

Previous studies show that B. thetaiotaomicron stimulates angiogenesis, which is the formation of new blood vessels, during intestinal development following birth. These studies used germ-free mice in order to control the microbiota and inoculated the mice with a specific bacteria, B. thetaiotaomicron. Angiogenesis further benefits the host by increasing the human's ability to absorb the nutrients that the microbe assists in produce.[1]

B. thetaiotaomicron dominates the intestinal microbiome and also aids in another postnatal development of the gut with the formation of the mucosal barrier in the intestine, which plays a major role in maintaining host-microbiota homeostasis.[14][15] The mucosal barrier, located between the intestinal epithelium and microbiota, is semipermeable, allowing the uptake of essential nutrients while restricting the passage of pathogenic molecules.[14][16] Nearly 90% of the bacteria within the gut microbiota, colonizing the gastrointestinal tract (GIT), belongs to the Bacteroidetes or Firmicutes phyla.[14] B. thetaiotaomicron's ability to grow on host-derived polysaccharides in mucus is a major contributor to its persistence in the GIT.[14] 

Role in immune response

B. thetaiotaomicron is a prominent member of the human gut microbiota, and its role in the immune response is complex. The interaction between B. thetaiotaomicron and the immune system contributes to the maintenance of gut homeostasis and the development of an immune system. The anti-inflammatory and immunomodulatory characteristics of extracellular vesicles generated by the prevalent human gut bacteria B. thetaiotaomicron are evident, along with the identification of the molecular mechanisms governing their interaction with innate immune cells.[17] B.thetaiotaomicron has been associated with other commensal bacteria and the induction of regulatory T cells which are essential for maintaining immune tolerance and preventing excessive inflammatory response.[18][19]

The outer membrane vesicles (OMVs) not only aid in protecting B. thetaiotaomicron from degradation, but also play a major role in promoting regulatory dendritic cell responses. OMVs of B. thetaiotaomicron in a healthy gut stimulate colonic dendritic cells (DC) to express IL-10. T-cells are stimulated by IL-10 and is expressed via the innate immune system through macrophages and DC. B. thetaiotaomicron OMVs in individuals with ulcerative colitis (UC) and Crohn's disease (CD) are unable to stimulate IL-10 expression, resulting in a loss of regulatory DC. In these diseases, B. thetaiotaomicron OMVs also cause a significantly lower amount of DC to be expressed. These results were also observed in patients with the inactive diseases, signifying that the defects in immune response are intrinsic in inflammatory bowel disease (IBD).[20]

Pathology

B. thetaiotaomicron is also an opportunistic pathogen and can infect tissues exposed to gut flora.[13] While contained in the gut, B. thetaiotaomicron generally maintains a beneficial relationship with its host. However, the bacteria can cause serious pathology when it is present in an inappropriate environment. Bacteria can escape the gut as a result of a rupture of the gastrointestinal tract. This can lead to diseases like bacteremia, which is the presence of bacteria in the bloodstream. It can also lead to abscess formation, which occurs when an area of tissue is infected and the body's immune system sends white blood cells to try to fight and contain it.[7]

Its polysaccharide-metabolizing abilities make it a food source for other components of the gut microbiome. For example, while B. thetaiotaomicron expresses sialidase enzymes, it cannot catabolize sialic acid; as a result its presence increases the free sialic acid available for other organisms in the gut to use as an energy source. These interactions can contribute to the growth of pathogenic bacteria such as Clostridium difficile, which uses sialic acid as a carbon source.[21] Similar interactions can cause B. thetaiotaomicron to exacerbate pathogenic E. coli infection.[22] These strategies allow B. thetaiotaomicron to further thrive in the competitive environment of the human intestine.

References

  1. 1 2 3 4 5 6 7 8 9 10 11 Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, et al. (March 2003). "A genomic view of the human-Bacteroides thetaiotaomicron symbiosis". Science. 299 (5615): 2074–2076. Bibcode:2003Sci...299.2074X. doi:10.1126/science.1080029. PMID 12663928. S2CID 34071235.
  2. 1 2 Ryan D, Jenniches L, Reichardt S, Barquist L, Westermann AJ (July 2020). "A high-resolution transcriptome map identifies small RNA regulation of metabolism in the gut microbe Bacteroides thetaiotaomicron". Nature Communications. 11 (1): 3557. Bibcode:2020NatCo..11.3557R. doi:10.1038/s41467-020-17348-5. PMC 7366714. PMID 32678091.
  3. 1 2 "Bacteroides". List of Prokaryotic names with Standing in Nomenclature. Retrieved 20 May 2018.
  4. ↑ Hahnke RL, Meier-Kolthoff JP, García-López M, Mukherjee S, Huntemann M, Ivanova NN, et al. (2016-12-20). "Genome-Based Taxonomic Classification of Bacteroidetes". Frontiers in Microbiology. 7: 2003. doi:10.3389/fmicb.2016.02003. PMC 5167729. PMID 28066339.
  5. ↑ Oren A, Vandamme P, Schink B (June 2016). "Notes on the use of Greek word roots in genus and species names of prokaryotes". International Journal of Systematic and Evolutionary Microbiology. 66 (6): 2129–2140. doi:10.1099/ijsem.0.001063. PMID 27055242.
  6. ↑ Trüper HG (April 1999). "How to name a prokaryote?: Etymological considerations, proposals and practical advice in prokaryote nomenclature". FEMS Microbiology Reviews. 23 (2): 231–249. doi:10.1111/j.1574-6976.1999.tb00397.x.
  7. 1 2 3 4 Wexler HM (October 2007). "Bacteroides: the good, the bad, and the nitty-gritty". Clinical Microbiology Reviews. 20 (4): 593–621. doi:10.1128/CMR.00008-07. PMC 2176045. PMID 17934076.
  8. 1 2 3 Xu J, Chiang HC, Bjursell MK, Gordon JI (January 2004). "Message from a human gut symbiont: sensitivity is a prerequisite for sharing". Trends in Microbiology. 12 (1): 21–28. doi:10.1016/j.tim.2003.11.007. PMID 14700548.
  9. ↑ Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (February 2008). "Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis". Nature Reviews. Microbiology. 6 (2): 121–131. doi:10.1038/nrmicro1817. PMID 18180751. S2CID 10400358.
  10. ↑ Sonnenburg JL, Xu J, Leip DD, Chen CH, Westover BP, Weatherford J, et al. (March 2005). "Glycan foraging in vivo by an intestine-adapted bacterial symbiont". Science. 307 (5717): 1955–1959. Bibcode:2005Sci...307.1955S. doi:10.1126/science.1109051. PMID 15790854. S2CID 13588903.
  11. 1 2 3 4 5 6 Comstock LE, Coyne MJ (October 2003). "Bacteroides thetaiotaomicron: a dynamic, niche-adapted human symbiont". BioEssays. 25 (10): 926–929. doi:10.1002/bies.10350. PMID 14505359.
  12. 1 2 Trovão F, Correia VG, Lourenço FM, Ribeiro DO, Carvalho AL, Palma AS, Pinheiro BA (2023-01-02). "The structure of a Bacteroides thetaiotaomicron carbohydrate-binding module provides new insight into the recognition of complex pectic polysaccharides by the human microbiome". Journal of Structural Biology. 7: 100084. doi:10.1016/j.yjsbx.2022.100084. PMC 9843283. PMID 36660365.
  13. 1 2 3 4 Mishra S, Imlay JA (December 2013). "An anaerobic bacterium, Bacteroides thetaiotaomicron, uses a consortium of enzymes to scavenge hydrogen peroxide". Molecular Microbiology. 90 (6): 1356–1371. doi:10.1111/mmi.12438. PMC 3882148. PMID 24164536.
  14. 1 2 3 4 Wrzosek L, Miquel S, Noordine ML, Bouet S, Joncquel Chevalier-Curt M, Robert V, et al. (May 2013). "Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent". BMC Biology. 11: 61. doi:10.1186/1741-7007-11-61. PMC 3673873. PMID 23692866.
  15. ↑ Xu J, Gordon JI (September 2003). "Honor thy symbionts". Proceedings of the National Academy of Sciences of the United States of America. 100 (18): 10452–10459. doi:10.1073/pnas.1734063100. PMC 193582. PMID 12923294.
  16. ↑ Vancamelbeke M, Vermeire S (September 2017). "The intestinal barrier: a fundamental role in health and disease". Expert Review of Gastroenterology & Hepatology. 11 (9): 821–834. doi:10.1080/17474124.2017.1343143. PMC 6104804. PMID 28650209.
  17. ↑ Fonseca S, Carvalho AL, Miquel-Clopés A, Jones EJ, Juodeikis R, Stentz R, Carding SR (2022-11-10). "Extracellular vesicles produced by the human gut commensal bacterium Bacteroides thetaiotaomicron elicit anti-inflammatory responses from innate immune cells". Frontiers in Microbiology. 13: 1050271. doi:10.3389/fmicb.2022.1050271. PMC 9684339. PMID 36439842.
  18. ↑ Wegorzewska MM, Glowacki RW, Hsieh SA, Donermeyer DL, Hickey CA, Horvath SC, et al. (February 2019). "Diet modulates colonic T cell responses by regulating the expression of a Bacteroides thetaiotaomicron antigen". Science Immunology. 4 (32). doi:10.1126/sciimmunol.aau9079. PMC 6550999. PMID 30737355.
  19. ↑ Wu, Hsin-Jung; Wu, Eric (January 2012). "The role of gut microbiota in immune homeostasis and autoimmunity". Gut Microbes. 3 (1): 4–14. doi:10.4161/gmic.19320. ISSN 1949-0976. PMC 3337124.
  20. ↑ Durant L, Stentz R, Noble A, Brooks J, Gicheva N, Reddi D, et al. (June 2020). "Bacteroides thetaiotaomicron-derived outer membrane vesicles promote regulatory dendritic cell responses in health but not in inflammatory bowel disease". Microbiome. 8 (1): 88. doi:10.1186/s40168-020-00868-z. PMC 7282036. PMID 32513301.
  21. ↑ Bäumler AJ, Sperandio V (July 2016). "Interactions between the microbiota and pathogenic bacteria in the gut". Nature. 535 (7610): 85–93. Bibcode:2016Natur.535...85B. doi:10.1038/nature18849. PMC 5114849. PMID 27383983.
  22. ↑ Curtis MM, Hu Z, Klimko C, Narayanan S, Deberardinis R, Sperandio V (December 2014). "The gut commensal Bacteroides thetaiotaomicron exacerbates enteric infection through modification of the metabolic landscape". Cell Host & Microbe. 16 (6): 759–769. doi:10.1016/j.chom.2014.11.005. PMC 4269104. PMID 25498343.
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