Phocaeicola vulgatus
Scientific classification Edit this classification
Domain: Bacteria
Phylum: Bacteroidota
Class: Bacteroidia
Order: Bacteroidales
Family: Bacteroidaceae
Genus: Phocaeicola
Species:
P. vulgatus
Binomial name
Phocaeicola vulgatus
García-López et al. 2020

Phocaeicola vulgatus, (formerly Bacteroides vulgatus),[1] is a mutualistic anaerobic Gram negative rod bacteria commonly found in the human gut microbiome and isolated from feces.[2] P. vulgatus has medical relevance and has been notable in scientific research due to its production of fatty acids, potential use as a probiotic, and associations with protecting against and worsening some inflammatory diseases.[3][4][5] Due to the difficulties in culturing anaerobic bacteria, P. vulgatus is still highly uncharacterised so efforts are being made to make use of multi-omic approaches to investigate the human gut microbiome more thoroughly in hopes to fully understand the role of this species in the development of and protection against diseases, as well as its potential uses in medicine and research.[6] Generally, P. vulgatus is considered as a beneficial bacteria that contributes to digestion and a balanced microbiome, but it has been known to cause opportunistic infections and induce or worsen inflammatory responses. Due to its abundance in the microbiome, some researchers are investigating these species in hopes that it will be a suitable model organism for gut microbiome research, like Bacteroides thetaiotaomicron.

Biology and biochemistry

P. vulgatus does not form spores and is able to grow in mesophilic conditions (37 °C), it is an anaerobe with a DNA GC content of around 41–42%.[7] P. vulgatus is one of the more predominant species in the Bacteroidaceae family, which are one of the five main genera in the human gut microbiome, Bacteroidaceae make up around 30% of fecal isolates.[8] P. vulgatus is found globally and most samples have been isolated from humans.[7] P. vulgatus has more rarely been isolated from companion animals like dogs and cats, and also from sewage, sediment, farms, and plants.[9]

Global distribution of 16S sequence AB510712 Phocaeicola vulgatus subclade from BacDrive, made with Microbeatlas 1.0

Structure and metabolism

P. vulgatus is a Gram negative rod bacterium. The structure and metabolism of P. vulgatus is still not fully understood, but it is known that P. vulgatus is indole and urea negative and is capable of growing on a range of sugars, the most notable carbon source being glucose.[10][7] A nitrogen source is also required, with its preferred source being ammonia.[10] In regards to its cell membrane, the species has a lipopolysaccharide structure consisting of a mix of penta- and tetra-acylated mono-phosphorylated molecules,[11] and P. vulgatus produces RagB/SusD protein which is an outer membrane family of proteins involved in bacterial nutrient uptake.[12]

Culturing

P. vulgatus is a biosafety level 1 organism that can be grown in anaerobic laboratory conditions at 37 °C with a growth time of 1–2 days.[7] P. vulgatus can be exposed to 0.03% dissolved oxygen with no effect on growth, and it is believed that anaerobes like P. vulgatus possess specific mechanisms to survive or cope with small levels of oxygen in the environment.[13] A variety of liquid and solid media can be used to grow P. vulgatus, some of these include; chopped meat media supplemented with haemine 5μg/ml and Vitamin K1, columbia blood media, fastidious anaerobe broth, brain heart influsion media, and tryptone yeast extract with glucose media.[14][15][10] It is recommended to grow anaerobic bacteria like P. vulgatus in an anaerobic chamber, glove box, anaerobic jar, or with the use of Hungate tubes, syringes, and resazurin oxygen indicator.[10] It is also recommended to grow strains in media with the addition of Vitamin B12 and NaHCO3 to ensure cell survival.[10]

Diversity

Phylogeny and taxonomy

P. vulgatus belongs to the Bacteroidaceae family and was formerly considered to be part of the Bacteroides genus, but was reclassified in 2020 to the Phocaeicola genus. This was due to phylogenetic analysis suggesting it to be more closely related to the Phocaeicola genus than to B. fragilis.[1] B. barnesiae, B. caecicola, B. caecigallinarum, B. chincillae, B. coprocola, B. coprophilus, B. dorei, B. gallinaceum, B. massiliensis, B. paurosaccharolyticus, B. plebeius, B. salanitronis, B. sartorii were all reclassified to Phocaeicola at the same time.[1] P. vulgatus is often hard to distinguish from its close relative, P. dorei, through matrix-assisted laser desorption/ionization identification, so 16S sequencing is used.[16]

The name Phocaeicola was first proposed in 2009 when a bacteria known as Phocaeicola abscessus was isolated from the brain of a man from the town Foça, which was known as Phocaea in the 11th century BC. The name vulgatus comes from the Latin vulgatus, meaning common or popular.[17][18]

Type strain

The type strain for this species is Phocaeicola vulgatus ATCC 8482.[19]

Genomics

Genome

The genome of P. vulgatus is around 5Mbp in length.[20]

Plasmids

Some strains of P. vulgatus and its close relative P. dorei have been know to carry a plasmid (called pBUN24) of around 9Kbp which is the vector for its toxin, BcpT.[21] A version of this plasmid is also found in B. uniformis at around 90% similarity. Some cases have seen this plasmid present in isolates of P. vulgatus, B. intestinalis, and P. distasonis from the same individual, suggesting that the plasmid is mobilisable between multiple species of bacteria.[21]

The plasmid pBI143 has been identified to be mobilisable to P. vulgatus, this plasmid was first identified in 1985 in Bacteroides fragilis.[22][23]

Role in the gut microbiome

P. vulgatus seems to be present from early in an individuals development, and abundance is affected by type of diet the neonate has – formular or milk.[24] Studies suggest that P. vulgatus is important in breaking down the complex carbohydrates in breast milk and therefore may be more abundant in babies who are breastfed. Infants as young at 2 months have been found to have species of Bacteroidaceae in their fecal microbiome.[25]

P. vulgatus becomes more abundant as a human ages[24] and will be involved in breakdown and digestion of other foods in the human diet, as well as the production of important molecules needed by the human body.[26][27] It is capable of degrading complex heteropolysaccharides, like xylan into small chain fatty acids to be used in the human body. P. vulgatus also possess the ldh gene, which codes for the production of D-lactate dehydrogenase, an enzyme that is responsible for the conversion of lactate into pyruvate.[28] These are important metabolic fuels for the function of mitochrondria in cells in the body.[29][30] P. vulgatus is also known to produce acetate, and succinate from hexose sugars as well as being involved in synthesising vitamins and bioactive compounds.[31][28]

Antibacterial toxin

This bacteria likely has a very complex role in the microbiome and interacts with many of the species present. Exposure to treatment that lowers the abundance of E. coli and C. sporogenes increases abundance of P. vulgatus P. vulgatus produces an antibacterial protein called BcpT which is encoded on a small conjugative plasmid.[21] This protein's receptor is Lipid A-core glycan which is found in other Bacteroidales families. The protein has a unique structure, unlike other characterised toxin proteins and it requires a two site cleavage to activate its antibacterial activity. Due to this, it is suggested to be a newly identified family of antibacterial toxins found in the gut microbiome.[21] Bacteria will often produce toxins like these in order to pose a threat to other bacteria competing for the same niche, in doing this they will kill or inhibiting growth of these competitors, and therefore gain the nutrients and habitats[32]

Role in disease

Irritable bowel disease

Higher levels of dipeptides and oligopeptides have been observed in fecal samples from ulcerative colitis patients, and are believed to be due to an overproduction of proteases from P. vulgatus and related species.[6] In a study looking at investigating this observation by investigating the transepithelial electrical resistance, which is a reliable method for testing the integrity of a cell monolayer,[33] in the presence of these peptides from P. vulgatus. They saw that mouse epithelial layer integrity was lower in the presence of the proteases from P. vulgatus, hinting to damage of the intestinal wall, and saw that this was significantly reduced when a protease inhibitor was given to the mouse.[6] Other work has seen similar results to this in rats.[34] Ulcerative colitis has also been seen to be induced more severely in guinea pigs exposed to both P. vulgatus and carrageenan, a polysaccharide found in red seaweed that is known to induce inflammation and worsen symptoms of ulcerative colitis,[35][36] animals exposed to just P. vulgatus showed no signs of ulcerative colitis unless exposure was daily, in which smaller signs of inflammation were observed in the epithelium.

While some research has shown P. vulgatus plays a role in worsening symptoms of irritable bowel diseases, a study expanding on previous findings that E. coli Nissle could act as a probiotic, protecting against ulcerative colitis,[37][38] found that P. vulgatus had the same impact as E. coli Nissle and reduced diseases expression in IL-2-/- mice[39]

Obesity

P. vulgatus is reported to be a member of the healthy microbiota, preventing obesity phenotypes from worsening in some studies[40]

Role in biotechnology

While P. vulgatus does prefer anaerobic conditions, it is capable of surviving exposure to oxygen for short periods of time.,[8][13] and is known to produce very little gas during growth, the gas it produces is hydrogen.[41] Due to its low hydrogen production, P. vulgatus has been used in developing gas production measuring systems in biotechnology, allowing for testing the lower detection limits of gas sensors[3]

History

P. vulgatus was first described in 1932 by Arnold H. Eggerth and Bernard H. Gagnon.[2] In this study, it was recognised that P. vulgatus was very common compared to other species isolated from human feces, and made up the majority of the isolates in this study.

References

  1. 1 2 3 García-López, Marina; Meier-Kolthoff, Jan P.; Tindall, Brian J.; Gronow, Sabine; Woyke, Tanja; Kyrpides, Nikos C.; Hahnke, Richard L.; Göker, Markus (2019-09-23). "Analysis of 1,000 Type-Strain Genomes Improves Taxonomic Classification of Bacteroidetes". Frontiers in Microbiology. 10: 2083. doi:10.3389/fmicb.2019.02083. ISSN 1664-302X. PMC 6767994. PMID 31608019.
  2. 1 2 Eggerth, Arnold H.; Gagnon, Bernard H. (April 1933). "The Bacteroides of Human Feces". Journal of Bacteriology. 25 (4): 389–413. doi:10.1128/jb.25.4.389-413.1933. ISSN 0021-9193. PMC 533498. PMID 16559622.
  3. 1 2 Miebach, Katharina; Finger, Maurice; Scherer, Alexandra Maria Katarina; Maaß, Constantin Alexander; Büchs, Jochen (2023-07-18). "Hydrogen online monitoring based on thermal conductivity for anaerobic microorganisms". Biotechnology and Bioengineering. 120 (8): 2199–2213. doi:10.1002/bit.28502. ISSN 0006-3592. PMID 37462090. S2CID 259948317.
  4. ↑ Noor, Samah O; Ridgway, Karyn; Scovell, Louise; Kemsley, E Katherine; Lund, Elizabeth K; Jamieson, Crawford; Johnson, Ian T; Narbad, Arjan (December 2010). "Ulcerative colitis and irritable bowel patients exhibit distinct abnormalities of the gut microbiota". BMC Gastroenterology. 10 (1): 134. doi:10.1186/1471-230X-10-134. ISSN 1471-230X. PMC 3002299. PMID 21073731.
  5. ↑ Kang, Xing; Ng, Siu-Kin; Liu, Changan; Lin, Yufeng; Zhou, Yunfei; Kwong, Thomas N.Y.; Ni, Yunbi; Lam, Thomas Y.T.; Wu, William K.K.; Wei, Hong; Sung, Joseph J.Y.; Yu, Jun; Wong, Sunny H. (July 2023). "Altered gut microbiota of obesity subjects promotes colorectal carcinogenesis in mice". eBioMedicine. 93: 104670. doi:10.1016/j.ebiom.2023.104670. PMC 10314234. PMID 37343363.
  6. 1 2 3 Mills, Robert H.; Dulai, Parambir S.; Vázquez-Baeza, Yoshiki; Sauceda, Consuelo; Daniel, Noëmie; Gerner, Romana R.; Batachari, Lakshmi E.; Malfavon, Mario; Zhu, Qiyun; Weldon, Kelly; Humphrey, Greg; Carrillo-Terrazas, Marvic; Goldasich, Lindsay DeRight; Bryant, MacKenzie; Raffatellu, Manuela (2022-01-27). "Multi-omics analyses of the ulcerative colitis gut microbiome link Bacteroides vulgatus proteases with disease severity". Nature Microbiology. 7 (2): 262–276. doi:10.1038/s41564-021-01050-3. ISSN 2058-5276. PMC 8852248. PMID 35087228.
  7. 1 2 3 4 Podstawka, Adam. "Phocaeicola vulgatus | Type strain | DSM 1447, ATCC 8482, CCUG 4940, JCM 5826, BCRC 12903, CIP 103714, IAM 14520, IFO 14291, LMG 7956, NBRC 14291, NCTC 11154 | BacDiveID:1601". bacdive.dsmz.de. Retrieved 2023-07-24.
  8. 1 2 Salyers, A.A (1984). "Bacteroides of the human lower intestinal tract". Annual Review of Microbiology. 38: 293–313. doi:10.1146/annurev.mi.38.100184.001453. PMID 6388494.
  9. ↑ "microbeAtlas". microbeatlas.org. Retrieved 2023-07-27.
  10. 1 2 3 4 5 Bacic, Melissa K.; Smith, C. Jeffrey (May 2008). "Laboratory Maintenance and Cultivation of Bacteroides Species". Current Protocols in Microbiology. 9 (1): Unit 13C.1. doi:10.1002/9780471729259.mc13c01s9. ISSN 1934-8525. PMC 3836205. PMID 18770533.
  11. ↑ Di Lorenzo, Flaviana; Pither, Molly D.; Martufi, Michela; Scarinci, Ilaria; Guzmán-Caldentey, Joan; Łakomiec, Ewelina; Jachymek, Wojciech; Bruijns, Sven C. M.; Santamaría, Sonsoles Martín; Frick, Julia-Stephanie; van Kooyk, Yvette; Chiodo, Fabrizio; Silipo, Alba; Bernardini, Maria Lina; Molinaro, Antonio (2020-07-30). "Pairing Bacteroides vulgatus LPS Structure with Its Immunomodulatory Effects on Human Cellular Models". ACS Central Science. 6 (9): 1602–1616. doi:10.1021/acscentsci.0c00791. hdl:10261/217456. ISSN 2374-7943. PMC 7517413. PMID 32999936. S2CID 221997066.
  12. ↑ "UniProt". www.uniprot.org. Retrieved 2023-07-28.
  13. 1 2 Lu, Zheng; Imlay, James A. (2021-06-28). "When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence". Nature Reviews Microbiology. 19 (12): 774–785. doi:10.1038/s41579-021-00583-y. ISSN 1740-1526. PMC 9191689. PMID 34183820.
  14. ↑ "German Collection of Microorganisms and Cell Cultures GmbH: Details". www.dsmz.de. Retrieved 2023-07-25.
  15. ↑ Cato, E. P.; Johnson, J. L. (1976-04-01). "Reinstatement of Species Rank for Bacteroides fragilis, B. ovatus, B. distasonis, B. thetaiotaomicron, and B. vulgatus: Designation of Neotype Strains for Bacteroides fragilis (Veillon and Zuber) Castellani and Chalmers and Bacteroides thetaiotaomicron (Distaso) Castellani and Chalmers". International Journal of Systematic Bacteriology. 26 (2): 230–237. doi:10.1099/00207713-26-2-230. ISSN 0020-7713.
  16. ↑ Wexler, Hannah M. (2014), "The Genus Bacteroides", The Prokaryotes, Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 459–484, doi:10.1007/978-3-642-38954-2_129, ISBN 978-3-642-38953-5, retrieved 2023-07-26
  17. ↑ "Species: Phocaeicola vulgatus". lpsn.dsmz.de. Retrieved 2023-07-28.
  18. ↑ "Genus: Phocaeicola". lpsn.dsmz.de. Retrieved 2023-07-28.
  19. ↑ taxonomy. "Taxonomy browser (Phocaeicola vulgatus ATCC 8482)". www.ncbi.nlm.nih.gov. Retrieved 2023-07-28.
  20. ↑ Vu, Hanh; Muto, Yoshinori; Hayashi, Masahiro; Noguchi, Hideki; Tanaka, Kaori; Yamamoto, Yoshimasa (2022-02-17). "Complete Genome Sequences of Three Phocaeicola vulgatus Strains Isolated from a Healthy Japanese Individual". Microbiology Resource Announcements. 11 (2): e0112421. doi:10.1128/mra.01124-21. ISSN 2576-098X. PMC 8812301. PMID 35112912.
  21. 1 2 3 4 Evans, Jordan C.; McEneany, Valentina Laclare; Coyne, Michael J.; Caldwell, Elizabeth P.; Sheahan, Madeline L.; Von, Salena S.; Coyne, Emily M.; Tweten, Rodney K.; Comstock, Laurie E. (2022-07-23). "A proteolytically activated antimicrobial toxin encoded on a mobile plasmid of Bacteroidales induces a protective response". Nature Communications. 13 (1): 4258. Bibcode:2022NatCo..13.4258E. doi:10.1038/s41467-022-31925-w. ISSN 2041-1723. PMC 9308784. PMID 35871068.
  22. ↑ Smith, C J (October 1985). "Development and use of cloning systems for Bacteroides fragilis: cloning of a plasmid-encoded clindamycin resistance determinant". Journal of Bacteriology. 164 (1): 294–301. doi:10.1128/jb.164.1.294-301.1985. ISSN 0021-9193. PMC 214243. PMID 2995313.
  23. ↑ Fogarty, Emily C; Schechter, Matthew S; Lolans, Karen; Sheahan, Madeline L.; Veseli, Iva; Moore, Ryan; Kiefl, Evan; Moody, Thomas; Rice, Phoebe A (2023-03-25). "A highly conserved and globally prevalent cryptic plasmid is among the most numerous mobile genetic elements in the human gut". BioRxiv: The Preprint Server for Biology. doi:10.1101/2023.03.25.534219. PMC 10055365. PMID 36993556. Retrieved 2023-07-28.
  24. 1 2 Rosa, Fernanda; Zybailov, Boris L.; Glazko, Galina V.; Rahmatallah, Yasir; Byrum, Stephanie; Mackintosh, Samuel G.; Bowlin, Anne K.; Yeruva, Laxmi (2021-10-22). "Milk Formula Diet Alters Bacterial and Host Protein Profile in Comparison to Human Milk Diet in Neonatal Piglet Model". Nutrients. 13 (11): 3718. doi:10.3390/nu13113718. ISSN 2072-6643. PMC 8618976. PMID 34835974.
  25. ↑ Cortes, Laetitia; Wopereis, Harm; Tartiere, Aude; Piquenot, Julie; Gouw, Joost; Tims, Sebastian; Knol, Jan; Chelsky, Daniel (2019-03-21). "Metaproteomic and 16S rRNA Gene Sequencing Analysis of the Infant Fecal Microbiome". International Journal of Molecular Sciences. 20 (6): 1430. doi:10.3390/ijms20061430. ISSN 1422-0067. PMC 6471839. PMID 30901843.
  26. ↑ LLC, HealthMatters io. "Phocaeicola vulgatus | Healthmatters.io". healthmatters.io. Retrieved 2023-07-28.
  27. ↑ Wexler, Aaron G.; Goodman, Andrew L. (2017-04-25). "An insider's perspective: Bacteroides as a window into the microbiome". Nature Microbiology. 2 (5): 17026. doi:10.1038/nmicrobiol.2017.26. ISSN 2058-5276. PMC 5679392. PMID 28440278.
  28. 1 2 Lück, Rebecca; Deppenmeier, Uwe (2022-01-26). "Genetic tools for the redirection of the central carbon flow towards the production of lactate in the human gut bacterium Phocaeicola (Bacteroides) vulgatus". Applied Microbiology and Biotechnology. 106 (3): 1211–1225. doi:10.1007/s00253-022-11777-6. ISSN 0175-7598. PMC 8816746. PMID 35080666.
  29. ↑ Gray, Lawrence R.; Tompkins, Sean C.; Taylor, Eric B. (2013-12-21). "Regulation of pyruvate metabolism and human disease". Cellular and Molecular Life Sciences. 71 (14): 2577–2604. doi:10.1007/s00018-013-1539-2. ISSN 1420-682X. PMC 4059968. PMID 24363178.
  30. ↑ Lee, Tae-Yoon (2021-07-31). "Lactate: a multifunctional signaling molecule". Yeungnam University Journal of Medicine. 38 (3): 183–193. doi:10.12701/yujm.2020.00892. ISSN 2384-0293. PMC 8225492. PMID 33596629.
  31. ↑ Flint, Harry J.; Duncan, Sylvia H.; Scott, Karen P.; Louis, Petra (2014-09-30). "Links between diet, gut microbiota composition and gut metabolism". Proceedings of the Nutrition Society. 74 (1): 13–22. doi:10.1017/s0029665114001463. ISSN 0029-6651. PMID 25268552. S2CID 206244014.
  32. ↑ Williams; Clarke (July 1998). "Why do microbes have toxins?". Journal of Applied Microbiology. 84 (S1): 1S–6S. doi:10.1046/j.1365-2672.1998.0840s101s.x. ISSN 1364-5072. PMID 9750356. S2CID 924506.
  33. ↑ Srinivasan, Balaji; Kolli, Aditya Reddy; Esch, Mandy Brigitte; Abaci, Hasan Erbil; Shuler, Michael L.; Hickman, James J. (April 2015). "TEER Measurement Techniques for In Vitro Barrier Model Systems". SLAS Technology. 20 (2): 107–126. doi:10.1177/2211068214561025. PMC 4652793. PMID 25586998.
  34. ↑ Rath, Heiko C.; Wilson, Kenneth H.; Sartor, R. Balfour (June 1999). "Differential Induction of Colitis and Gastritis in HLA-B27 Transgenic Rats Selectively Colonized with Bacteroides vulgatus or Escherichia coli". Infection and Immunity. 67 (6): 2969–2974. doi:10.1128/iai.67.6.2969-2974.1999. ISSN 0019-9567. PMC 96608. PMID 10338507.
  35. ↑ Onderdonk, A B; Cisneros, R L; Bronson, R T (November 1983). "Enhancement of experimental ulcerative colitis by immunization with Bacteroides vulgatus". Infection and Immunity. 42 (2): 783–788. doi:10.1128/iai.42.2.783-788.1983. ISSN 0019-9567. PMC 264498. PMID 6642651.
  36. ↑ Bhattacharyya, Sumit; Shumard, Theresa; Xie, Hui; Dodda, Amar; Varady, Krista A.; Feferman, Leo; Halline, Allan G.; Goldstein, Jay L.; Hanauer, Stephen B.; Tobacman, Joanne K. (2017-03-31). "A randomized trial of the effects of the no-carrageenan diet on ulcerative colitis disease activity". Nutrition and Healthy Aging. 4 (2): 181–192. doi:10.3233/NHA-170023. PMC 5389019. PMID 28447072.
  37. ↑ Kruis, W.; SchüTz, E.; Fric, P.; Fixa, B.; Judmaier, G.; Stolte, M. (October 1997). "Double‐blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis". Alimentary Pharmacology & Therapeutics. 11 (5): 853–858. doi:10.1046/j.1365-2036.1997.00225.x. ISSN 0269-2813. PMID 9354192. S2CID 46066824.
  38. ↑ Rembacken, BJ; Snelling, AM; Hawkey, PM; Chalmers, DM; Axon, ATR (August 1999). "Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial". The Lancet. 354 (9179): 635–639. doi:10.1016/S0140-6736(98)06343-0. PMID 10466665. S2CID 41212300.
  39. ↑ Waidmann, Marc; Bechtold, Oliver; Frick, Julia-stefanie; Lehr, Hans-anton; Schubert, Sören; Dobrindt, Ulrich; Loeffler, Jürgen; Bohn, Erwin; Autenrieth, Ingo B (July 2003). "Bacteroides vulgatus protects against escherichia coli-induced colitis in gnotobiotic interleukin-2-deficient mice". Gastroenterology. 125 (1): 162–177. doi:10.1016/s0016-5085(03)00672-3. ISSN 0016-5085. PMID 12851881.
  40. ↑ Ridaura, Vanessa K.; Faith, Jeremiah J.; Rey, Federico E.; Cheng, Jiye; Duncan, Alexis E.; Kau, Andrew L.; Griffin, Nicholas W.; Lombard, Vincent; Henrissat, Bernard; Bain, James R.; Muehlbauer, Michael J.; Ilkayeva, Olga; Semenkovich, Clay F.; Funai, Katsuhiko; Hayashi, David K. (2013-09-06). "Gut Microbiota from Twins Discordant for Obesity Modulate Metabolism in Mice". Science. 341 (6150). doi:10.1126/science.1241214. ISSN 0036-8075. PMC 3829625. PMID 24009397.
  41. ↑ Kazimierowicz, Joanna; Dębowski, Marcin; Zieliński, Marcin (September 2022). "Effectiveness of Hydrogen Production by Bacteroides vulgatus in Psychrophilic Fermentation of Cattle Slurry". Clean Technologies. 4 (3): 806–814. doi:10.3390/cleantechnol4030049. ISSN 2571-8797.
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