Prevotella Explained

Prevotella is a genus of Gram-negative bacteria.

Prevotella species are widely distributed across varied ecological habitats, with 57 characterized species spanning both human and other mammalian hosts.[1] In mammals, this genus is notably prevalent in the swine gut microbiome.[2]

In humans, Prevotella species are members of the oral, vaginal, and gut microbiota and are often recovered from anaerobic infections of the respiratory tract. These infections include aspiration pneumonia, lung abscess, pulmonary empyema, and chronic otitis media and sinusitis. They have been isolated from abscesses and burns in the vicinity of the mouth, bites, paronychia, urinary tract infection, brain abscesses, osteomyelitis, and bacteremia associated with upper respiratory tract infections. Prevotella spp. predominate in periodontal disease and periodontal abscesses.[3]

Role in gut microbiota

The human gut is mainly inhabited by two phyla of bacteria—Bacillota and Bacteroidota, the latter mostly dominated by Bacteroides and Prevotella genera. Prevotella and Bacteroides are thought to have had a common ancestor.[4] Formally, the two genera were differentiated in 1990.[5] However classification is ongoing. For example, Bacteroides melaninogenicus has been reclassified and split into Prevotella melaninogenica and Prevotella intermedia.[6] Either Prevotella or Bacteroides dominate the gut and may be antagonistic. Prevotella is more common in non-Westernised populations consuming a plant-rich diet. In Western populations it has been associated with diets rich in fruits and vegetables. Genome analysis of Prevotella copri showed it was deficient in the ability to degrade host glycans and is more genetically equipped for plant glycan degradation. In a study of gut bacteria of children in Burkina Faso, Prevotella made up 53% of the gut bacteria but were absent in age-matched European children.[7]

Long-term diet is reported to be associated with gut microbiome composition—those who eat protein and animal fats have predominantly Bacteroides bacteria, while those who consume more carbohydrates, especially fibre, feature Prevotella species.[8]

Prevotella is associated with gut inflammation. Increased levels of P. copri might contribute to chronic inflammation in HIV patients. Single species isolate P. copri CB7 has been reported to be beneficial or detrimental, depending on context. The genus Prevotella exhibits significant genetic diversity, particularly between species associated with humans and those found in other animals. This diversity is highlighted by distinct evolutionary paths and genome sizes, with ranging base pair sizes and notable variation in G+C content. Human-related Prevotella species tend to group separately from those in animals such as swine and ruminants. In addition to genetic and overall microbiota differences, Prevotella's high genetic diversity makes it difficult to predict their function, which can vary across individuals.

There have also been studies uncovering the role of bacteriophages, including the discovery of megaphages in the large intestine associated with Prevotella, highlighting the potential for these phages to influence microbial populations within the host microbiome.[9]

Vaginal microbiota

Prevotella species may be commensal in the vagina, though increased abundance of Prevotella in vaginal mucosa is associated with bacterial vaginosis. A study of 542 Korean women, including identical and fraternal twins, highlighted that the vaginal microbiota's composition is influenced by menopausal status and bacterial vaginosis, with Lactobacillus and Prevotella being the most inheritable among beneficial and potentially harmful bacteria, respectively. An analysis pinpointed a genetic link between interleukin-5 variants and Prevotella abundance. Additionally, obesity was found to significantly diversify the vaginal microbiota, particularly increasing Prevotella presence. Other environmental factors like hormone therapy, human papillomavirus (HPV) infection can also influence the abundance of Prevotella.[10]

Prevotella bivia produces lipopolysaccharides and ammonia that are part of vaginal mucus. It is also associated with epithelial cytokine production and enhances the growth of other bacterial vaginosis-associated organisms, such as Gardnerella vaginalis. The latter in turn was found to stimulate growth of P. bivia.[11] P. bivia in the vaginal tract triggers an immune response similar to lipopolysaccharides, activating genes involved in the Th17 pathway (IL23A, IL6, IL1A, IL1B) through antigen-presenting cells. This activation leads to the recruitment of Th cells to the inflamed area, important for women's health since the presence of CCR5+ Th cells in the vaginal mucosa could increase HIV transmission risk during bacterial vaginosis.[12]

Pathogenicity

Prevotella intermedia and P. nigrescens are associated with inflammatory periodontal diseases, such as pregnancy gingivitis, acute necrotizing ulcerative gingivitis and adult periodontitis. Together with Porphyromonas gingivalis they are known as black-pigmenting anaerobes. All three require haemin to provide iron for their growth. These species were shown to bind lactoferrin that is released together with the contents of neutrophils during inflammation and bleeding in periodontitis patients. Lactoferrin inhibits the growth of P. gingivalis but not Prevotella.[13] Inorganic iron and iron-binding proteins such as transferrin and lactoferrin do not support the growth of P. intermedia, however hemin–iron-containing compounds which include hemin, human hemoglobin, bovine hemoglobin, and bovine catalase stimulate the growth of P. intermedia.[14] Hemoglobin-binding protein on the cell surface of P. intermedia has been described.[15]

Some studies have linked abnormal levels of Prevotella copri and rheumatoid arthritis.[16] [17]

An overgrowth of Prevotella and a reduction of Lactobacillus correlated with the onset of osteomyelitis in mice. The reduction of Prevotella in model mice led to an increase of Lactobacillus showing a protection effect against osteomyelitis. Thus, changes in the Prevotella microbiota may be related to the development of osteomyelitis.[18]

Approximately 70% and 30% of Prevotella are resistant to penicillin and clindamycin, respectively, while resistance to amoxicillin/clavulanate and metronidazole is reported in less than 10% of the clinical strains responsible for bloodstream infections in humans.[19]

Species

See also

Notes and References

  1. Tett . Adrian . Pasolli . Edoardo . Masetti . Giulia . Ercolini . Danilo . Segata . Nicola . September 2021 . Prevotella diversity, niches and interactions with the human host . Nature Reviews. Microbiology . 19 . 9 . 585–599 . 10.1038/s41579-021-00559-y . 1740-1534 . 34050328. 11572/316673 . free .
  2. Wang . Xiaofan . Tsai . Tsungcheng . Deng . Feilong . Wei . Xiaoyuan . Chai . Jianmin . Knapp . Joshua . Apple . Jason . Maxwell . Charles V. . Lee . Jung Ae . Li . Ying . Zhao . Jiangchao . 2019-07-30 . Longitudinal investigation of the swine gut microbiome from birth to market reveals stage and growth performance associated bacteria . Microbiome . 7 . 1 . 109 . 10.1186/s40168-019-0721-7 . free . 2049-2618 . 6664762 . 31362781.
  3. Tanaka S, Yoshida M, Murakami Y, etal . The relationship of Prevotella intermedia, Prevotella nigrescens and Prevotella melaninogenica in the supragingival plaque of children, caries and oral malodor . J Clin Pediatr Dent . 32 . 3 . 195–200 . 2008 . 18524268 . 10.17796/jcpd.32.3.vp657177815618l1. free .
  4. Ley. Ruth E.. February 2016. Gut microbiota in 2015: Prevotella in the gut: choose carefully. Nature Reviews. Gastroenterology & Hepatology. 13. 2. 69–70. 10.1038/nrgastro.2016.4. 1759-5053. 26828918. 30114888.
  5. Shah. H. N.. Collins. D. M.. April 1990. Prevotella, a new genus to include Bacteroides melaninogenicus and related species formerly classified in the genus Bacteroides. International Journal of Systematic Bacteriology. 40. 2. 205–208. 10.1099/00207713-40-2-205. 0020-7713. 2223612. free.
  6. Web site: Bacteroides Infection: Overview - eMedicine. 2008-12-11.
  7. 10.1073/pnas.1005963107. The impact of diet in shaping gut microbiota is revealed by a comparative study in children from Europe and rural Africa. 2010. De Filippo. C.. Cavalieri. D.. Di Paola. M.. Ramazzotti. M.. Poullet. J. B.. Massart. S.. Collini. S.. Pieraccini. G.. Lionetti. P.. Proceedings of the National Academy of Sciences. 107. 33. 14691–6. 20679230. 2930426. 2010PNAS..10714691D. free.
  8. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, Sinha R, Gilroy E, Gupta K, Baldassano R, Nessel L, Li H, Bushman FD, Lewis JD . Linking long-term dietary patterns with gut microbial enterotypes . Science . 334 . 6052 . 105–8 . October 7, 2011 . 3368382 . 21885731 . 10.1126/science.1208344 . 2011Sci...334..105W .
  9. Devoto . Audra E. . Santini . Joanne M. . Olm . Matthew R. . Anantharaman . Karthik . Munk . Patrick . Tung . Jenny . Archie . Elizabeth A. . Turnbaugh . Peter J. . Seed . Kimberley D. . Blekhman . Ran . Aarestrup . Frank M. . Thomas . Brian C. . Banfield . Jillian F. . April 2019 . Megaphages infect Prevotella and variants are widespread in gut microbiomes . Nature Microbiology . 4 . 4 . 693–700 . 10.1038/s41564-018-0338-9 . 2058-5276 . 6784885 . 30692672.
  10. Si . Jiyeon . You . Hyun Ju . Yu . Junsun . Sung . Joohon . Ko . GwangPyo . 2017-01-11 . Prevotella as a Hub for Vaginal Microbiota under the Influence of Host Genetics and Their Association with Obesity . Cell Host & Microbe . 21 . 1 . 97–105 . 10.1016/j.chom.2016.11.010 . 1934-6069 . 28017660. free .
  11. Randis . Tara M. . Ratner . Adam J. . 2019-02-01 . Gardnerella and Prevotella: Co-conspirators in the Pathogenesis of Bacterial Vaginosis . The Journal of Infectious Diseases . 220 . 7 . 1085–1088 . 10.1093/infdis/jiy705 . 1537-6613 . 6736359 . 30715397.
  12. Gosmann . Christina . Anahtar . Melis N. . Handley . Scott A. . Farcasanu . Mara . Abu-Ali . Galeb . Bowman . Brittany A. . Padavattan . Nikita . Desai . Chandni . Droit . Lindsay . Moodley . Amber . Dong . Mary . Chen . Yuezhou . Ismail . Nasreen . Ndung'u . Thumbi . Ghebremichael . Musie S. . 2017-01-17 . Lactobacillus-Deficient Cervicovaginal Bacterial Communities Are Associated with Increased HIV Acquisition in Young South African Women . Immunity . 46 . 1 . 29–37 . 10.1016/j.immuni.2016.12.013 . 1097-4180 . 5270628 . 28087240.
  13. Aguilera. O.. Andrés. M. T.. Heath. J.. Fierro. J. F.. Douglas. C. W.. May 1998. Evaluation of the antimicrobial effect of lactoferrin on Porphyromonas gingivalis, Prevotella intermedia and Prevotella nigrescens. FEMS Immunology and Medical Microbiology. 21. 1. 29–36. 10.1111/j.1574-695X.1998.tb01146.x. 0928-8244. 9657318. free.
  14. Folk. Shawn P.. Leung. K.-P.. 2002-03-01. Effects of porphyrins and inorganic iron on the growth of Prevotella intermedia. FEMS Microbiology Letters. 209. 1. 15–21. 10.1111/j.1574-6968.2002.tb11103.x. 12007648. 0378-1097. free.
  15. Shizukuishi. Satoshi. Minamino. Naoto. Kuboniwa. Masae. Maeda. Kazuhiko. Nagata. Hideki. Guan. Su-Min. 2004-06-01. Purification and characterization of a hemoglobin-binding outer membrane protein of Prevotella intermedia. FEMS Microbiology Letters. 235. 2. 333–339. 10.1111/j.1574-6968.2004.tb09607.x. 15183882. 0378-1097. free.
  16. Jose U Scher . Andrew Sczesnak . Randy S Longman . Nicola Segata . Carles Ubeda . Craig Bielski . Tim Rostron . Vincenzo Cerundolo . Eric G Pamer . Steven B Abramson . Curtis Huttenhower . Dan R Littman . Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis . eLife . November 5, 2013 . 2 . e01202 . 10.7554/eLife.01202 . 24192039 . 3816614 . free .
  17. Web site: Haridy . Rich . 2022-10-19 . New evidence linking gut bacteria with rheumatoid arthritis development . 2022-10-27 . New Atlas . en-US.
  18. Lukens. John R.. Gurung. Prajwal. Vogel. Peter. Johnson. Gordon R.. Carter. Robert A.. McGoldrick. Daniel J.. Bandi. Srinivasa Rao. Calabrese. Christopher R.. Walle. Lieselotte Vande. 2014-12-11. Dietary modulation of the microbiome affects autoinflammatory disease. Nature. 516. 7530. 246–249. 10.1038/nature13788. 0028-0836. 4268032. 25274309. 2014Natur.516..246L.
  19. Di Bella . Stefano . Antonello . Roberta Maria . Sanson . Gianfranco . Maraolo . Alberto Enrico . Giacobbe . Daniele Roberto . Sepulcri . Chiara . Ambretti . Simone . Aschbacher . Richard . Bartolini . Laura . Bernardo . Mariano . Bielli . Alessandra . June 2022 . Anaerobic bloodstream infections in Italy (ITANAEROBY): A 5-year retrospective nationwide survey . Anaerobe . en . 75 . 102583 . 10.1016/j.anaerobe.2022.102583. 35568274 . 248736289 . 11368/3020691 . free .

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