Gut Archaea in the context of human diseases

REVIEW ARTICLE

Gut Archaea in the context of human diseases

Agnieszka Krawczyk 1 , Dominika Salamon 1 , Kinga Kowalska-Duplaga 2 , Tomasz Gosiewski 3

1. Department of Molecular Medical Microbiology, Chair of Microbiology, Faculty of Medicine, Jagiellonian University Medical College, Krakow, Poland,
2. Department of Pediatrics, Gastroenterology and Nutrition, Faculty of Medicine, Jagiellonian University Medical College, Krakow, Poland,
3. Department of Microbiology, Jagiellonian University Medical College, Krakow, Poland,

Published: 2020-12-28
DOI: 10.5604/01.3001.0014.6166
GICID: 01.3001.0014.6166
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2020; 74 : 610-617

 

Abstract

Recently, thanks to the revolution of molecular biology techniques, there has been a rapid development of research on human intestinal microbiome. The use of modern molecular methods has confirmed that the human gastrointestinal tract is the habitat of a huge number of microorganisms forming a complex ecosystem. This ecosystem contains microorganisms belonging to three main domains: Bacteria, Archaea and Eukaryota, which play an important role in human health and disease. Recently, more and more evidence has emerged indicating the role of microorganisms in pathogenesis of multiple diseases. As a result of this, intestinal microorganisms have been recognized on the one hand as a factor that may be involved in inducing metabolic, inflammatory or neuropsychiatric diseases, and on the other hand as a potential therapeutic target. When considering the pathogenesis of specific diseases, most researchers focus primarily on the role of bacteria and fungi, while there are only few studies that include archaeons. These microorganisms, even though relatively small in number, may prove to be a key element in research on the role of the microbiome in the etiology of various diseases. The aim of this work is a systematic review of knowledge on the participation of intestinal archaeons in the course of selected diseases.

References

  • 1. Bang C., Weidenbach K., Gutsmann T., Heine H., Schmitz R.A.:The intestinal Archaea Methanosphaera stadtmanae and Methanobrevibactersmithii activate human dendritic cells. PLoS One,2014; 9: e99411
    Google Scholar
  • 2. Basseri R.J., Basseri B., Pimentel M., Chong K., Youdim A., Low K.,Hwang L., Soffer E., Chang C., Mathur R.: Intestinal methane productionin obese individuals is associated with a higher body massindex. Gastroenterol. Hepatol., 2012; 8: 22–28
    Google Scholar
  • 3. Blais Lecours P., Marsolais D., Cormier Y., Berberi M., HachéC., Bourdages R., Duchaine C.: Increased prevalence of Methanosphaerastadtmanae in inflammatory bowel diseases. PLoS One,2014; 9: e87734
    Google Scholar
  • 4. Brugère J.F., Borrel G., Gaci N., Tottey W., O’Toole P.W., Malpuech-Brugère C.: Archaebiotics: Proposed therapeutic use of archaea toprevent trimethylaminuria and cardiovascular disease. Gut Microbes,2014; 5: 5–10
    Google Scholar
  • 5. Chatterjee S., Park S., Low K., Kong Y., Pimentel M.: The degreeof breath methane production in IBS correlates with the severity ofconstipation. Am. J. Gastroenterol., 2007; 102: 837–841
    Google Scholar
  • 6. Cho Y.A., Lee J., Oh J.H., Chang H.J., Sohn D.K., Shin A., Kim J.:Genetic risk score, combined lifestyle factors and risk of colorectalcancer. Cancer Res. Treat., 2019; 51: 1033–1040
    Google Scholar
  • 7. Conway de Macario E., König H., Macario A.J., Kandler O.: Sixantigenic determinants in the surface layer of the archaebacteriumMethanococcus vannielii revealed by monoclonal antibodies. J. Immunol.,1984; 132: 883–887
    Google Scholar
  • 8. Ding L., Chang M., Guo Y., Zhang L., Xue C., Yanagita T., ZhangT., Wang Y.: Trimethylamine-N-oxide (TMAO)-induced atherosclerosisis associated with bile acid metabolism. Lipids Health Dis.,2018; 17: 286
    Google Scholar
  • 9. Dridi B., Henry M., El Khéchine A., Raoult D., Dran¬court M.: Highprevalence of Methanobrevibacter smithii and Methanosphaerastadtmanae detected in the human gut using an improved DNA detectionprotocol. PLoS One, 2009; 4: e7063
    Google Scholar
  • 10. Dridi B., Henry M., Richet H., Raoult D., Drancourt M.: Age-relatedprevalence of Methanomassiliicoccus luminyensis in the humangut microbiome. APMIS, 2012; 120: 773–777
    Google Scholar
  • 11. Dridi B., Raoult D., Drancourt M.: Archaea as emerging organismsin complex human microbiomes. Anaerobe, 2011; 17: 56–63
    Google Scholar
  • 12. Efenberger M., Wódz K., Brzezińska-Błaszczyk E.: Archeony –istotny składnik mikrobiomu człowieka. Prz. Lek., 2014; 71: 346–351
    Google Scholar
  • 13. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., HarpazN., Pace N.R.: Molecular-phylogenetic characterization of microbialcommunity imbalances in human inflammatory bowel diseases.Proc. Natl. Acad. Sci. USA, 2007; 104: 13780–13785
    Google Scholar
  • 14. Ghoshal U., Shukla R., Srivastava D., Ghoshal U.C.: Irritable bowelsyndrome, particularly the constipation-predominant form, involvesan increase in Methanobrevibacter smithii, which is associated withhiger methane production. Gut Liver, 2016; 10: 932–938
    Google Scholar
  • 15. Ghoshal U.C., Srivastava D., Misra A.: Sa1378 reduction of breathmethane using rifaximin shortens colon transit time and improvesconstipation: A randomized double-blind placebo controlled trial.Gastroenterology, 2015; 148: 308–309
    Google Scholar
  • 16. Ghoshal U.C., Srivastava D., Verma A., Misra A.: Slow transitconstipation associated with excess methane production and itsimprovement following rifaximin therapy: A case report. J. Neurogastroenterol.Motil., 2011; 17:185–188
    Google Scholar
  • 17. Gosiewski T., Strus M., Fyderek K., Kowalska-Duplaga K.,Wędrychowicz A., Jedynak-Wąsowicz U., Sładek M., PieczarkowskiS., Adamski P., Heczko P.B.: Horizontal distribution of the fecal microbiotain adolescents with inflammatory bowel disease. J. Pediatr.Gastroenterol. Nutr., 2012; 54: 20–27
    Google Scholar
  • 18. Grover M., Kanazawa M., Palsson O.S., Chitkara D.K., GangarosaL.M., Drossman D.A., Whitehead W.E.: Small intestinal bacterial overgrowthin irritable bowel syndrome: Association with colon motility,bowel symptoms, and psychological distress. Neurogastroenterol.Motil., 2008; 20: 998–1008
    Google Scholar
  • 19. Haines A., Metz G., Dilawari J., Blendis L., Wiggins H.: Breathmethanein patients with cancer of the large bowel. Lancet, 1977;2: 481–483
    Google Scholar
  • 20. Heidarian F., Alebouyeh M., Shahrokh S., Balaii H., Zali M.R.: Alteredfecal bacterial composition correlates with disease activity ininflammatory bowel disease and the extent of IL8 induction. Curr.Res. Transl. Med., 2019; 67: 41–50
    Google Scholar
  • 21. Hoffmann C., Dollive S., Grunberg S., Chen J., Li H., Wu G.D.,Lewis J.D., Bushman F.D.: Archaea and fungi of the human gut microbiome:Correlations with diet and bacterial residents. PLoS One,2013; 8: e66019
    Google Scholar
  • 22. Hwang L., Low K., Khoshini R., Melmed G., Sahakian A., MakhaniM., Pokkunuri V., Pimentel M.: Evaluating breath methane as a diagnostictest for constipation-predominant IBS. Dig. Dis. Sci., 2010;55: 398–440
    Google Scholar
  • 23. Joblin K.N., Naylor G.E., Williams A.G.: Effect of Methanobrevibactersmithii on xylanolytic activity of anaerobic ruminal fungi.Appl. Environ. Microbiol., 1990; 56: 2287–2295
    Google Scholar
  • 24. Keshavarzian A., Green S.J., Engen P.A., Voigt R.M., Naqib A., ForsythC.B., Mutlu E., Shannon K.M.: Colonic bacterial composition inParkinson’s disease. Mov. Disord., 2015; 30: 1351–1360
    Google Scholar
  • 25. Kim G., Deepinder F., Morales W., Hwang L., Weitsman S., ChangC., Gunsalus R., Pimentel M.: Methanobrevibater smithii is the predominantmethanogen in patients with consipation-predominantIBS and methane on breath. Dig. Dis. Sci., 2012; 57: 3213–3218
    Google Scholar
  • 26. Krawczyk A., Salamon D., Gosiewski T.: Role of gut microbiotain pathogenesis of selected chronic diseases. World Sci. News, 2019;132: 132–154
    Google Scholar
  • 27. Krawczyk A., Sroka-Oleksiak A., Kowalska-Duplaga K., FyderekK., Gosiewski T., Salamon D.: Impact of biological treatment on intestinalmicrobiom in children with Crohn’s disease. World Sci. News,2018; 104: 252–263
    Google Scholar
  • 28. Lacy B.E., Mearin F., Chang L., Chey W.D., Lembo A.J., Simren M.,Spiller R.: Bowel disorders. Gastroenterology, 2016; 150: 1393–1407
    Google Scholar
  • 29. Low K., Hwang L., Hua J., Zhu A., Morales W., Pimentel M.: Acombination of rifaximin and neomycin is most effective in treating irritable bowel syndrome patients with methane on lactulosebreath test. J. Clin. Gastroenterol., 2010; 44: 547–550
    Google Scholar
  • 30. Madore C., Leyrolle Q., Lacabanne C., Benmamar-Badel A., JoffreC., Nadjar A., Layé S.: Neuroinflammation in autism: Plausible roleof maternal inflammation, dietary omega 3, and microbiota. Neural.Plast., 2016; 2016: 3597209
    Google Scholar
  • 31. Majewska K., Szulińska M., Michałowska J., Markuszewski L.,Bogdański P.: Flora bakteryjna przewodu pokarmowego a chorobyukładu sercowo-naczyniowego. Forum Zaburzeń Metabolicznych,2017; 8: 1–6
    Google Scholar
  • 32. Majewski M., McCallum R.W.: Results of small intestinal bacterialovergrowth testing in irritable bowel syndrome patients: Clinicalprofiles and effects of antibiotic trial. Adv. Med. Sci., 2007; 52:139–142
    Google Scholar
  • 33. Mathur R., Amichai M., Mirocha J.M., Chua K., Basseri R.J., ChangC., Pimentel M.: Concomitant methane and hydrogen production inhumans is associated with a higher body mass index. Gastroenterology,2011; 140: S–335
    Google Scholar
  • 34. Mathur R., Kim G., Morales W., Sung J., Rooks E., Pokkunuri V.,Weitsman S., Barlow G.M., Chang C., Pimentel M.: Intestinal Methanobrevibactersmithii but not total bacteria is related to diet‐inducedweight gain in rats. Obesity, 2013; 21: 748–754
    Google Scholar
  • 35. Maukonen J., Kolho K.L., Paasela M., Honkanen J., Klemetti P.,Vaarala O., Saarela M.: Altered fecal microbiota in paediatric inflammatorybowel disease. J. Crohns Colitis, 2015; 9: 1088–1095
    Google Scholar
  • 36. Mbakwa C.A., Penders J., Savelkoul P.H., Thijs C., Dagnelie P.C.,Mommers M., Arts I.C.: Gut colonization with Methanobrevibactersmithii is associated with childhood weight development. Obesity,2015; 23: 2508–2516
    Google Scholar
  • 37. Mira-Pascual L., Cabrera-Rubio R., Ocon S., Costales P., Parra A.,Suarez A., Moris F., Rodrigo L., Mira A., Collado M.C.: Microbial mucosalcolonic shifts associated with the development of colorectalcancer reveal the presence of different bacterial and archeal biomarkers.J. Gastroenterol., 2015; 50: 167–179
    Google Scholar
  • 38. Pimentel M., Chatterjee S., Chow E.J., Park S., Kong Y.: Neomycinimproves constipation-predominant irritable bowel syndromein a fashion that is dependent on the presence of methane gas: Subanalysisof a double-blind randomized controlled study. Dig. Dis.Sci., 2006; 51: 1297–1301
    Google Scholar
  • 39. Pimentel M., Lin H.C., Enayati P., van den Burg B., Lee H.R.,Chen J.H., Park S., Kong Y., Conklin J.: Methane, a gas produced byenteric bacteria, slows intestinal transit and augments small intestinalcontractile activity. Am. J. Physiol. Gastrointest. Liver Physiol.,2006; 290: G1089–G1095
    Google Scholar
  • 40. Pimentel M., Mayer A.G., Park S., Chow E.J., Hasan A., Kong Y.:Methane production during lactulose breath test is associated withgastrointestinal disease presentation. Dig. Dis. Sci. 2003; 48: 86–92
    Google Scholar
  • 41. Piqué J.M., Pallarés M., Cusó E., Vilar-Bonet J., Gassull M.A.:Methane production and colon cancer. Gastroenterology, 1984; 87:601–605
    Google Scholar
  • 42. Ramezani A., Nolin T.D., Barrows I.R., Serrano M.G., Buck G.A.,Regunathan-Shenk R., West R.E.3rd, Latham P.S., Amdur R., Raj D.S.:Gut colonization with methanogenic archaea lowers plasma trimethylamineN-oxide concentrations in apolipoprotein e−/− mice.Sci. Rep., 2018; 8: 14752
    Google Scholar
  • 43. Rieu-Lesme F., Delbès C., Sollelis L.: Recovery of partial 16S rDNAsequences suggests the presence of Crenarchaeota in the human digestiveecosystem. Curr. Microbiol., 2005; 51: 317–321
    Google Scholar
  • 44. Salamon D., Sroka-Oleksiak A., Kapusta P., Szopa M., MrozińskaS., Ludwig-Słomczyńska A.H., Wołkow P.P., Bulanda M., Klupa T.,Małecki M.T., Gosiewski T.: Characteristics of gut microbiota in adultpatients with type 1 and type 2 diabetes based on next generationsequencing of the 16S rRNA gene fragment. Pol. Arch. Intern. Med.,2018; 128: 336–343
    Google Scholar
  • 45. Samuel B.S., Gordon J.I.: A humanized gnotobiotic mouse modelof host‐archaeal‐bacterial mutualism. Proc. Natl. Acad. Sci. USA,2006; 103: 10011‐10016
    Google Scholar
  • 46. Samuel B.S., Hansen E.E., Manchester J.K., Coutinho P.M., HenrissatB., Fulton R., Latreille P., Kim K., Wilson R.K., Gordon J.I.: Genomicand metabolic adaptations of Methanobrevibacter smithii to the humangut. Proc. Natl. Acad. Sci. USA, 2007; 104: 10643–10648
    Google Scholar
  • 47. Song N., Shin A., Jung H.S., Oh J.H., Kim J.: Effects of interactionsbetween common genetic variants and smoking on colorectal cancer.BMC Cancer, 2017; 17: 869
    Google Scholar
  • 48. Tan J., Chen Y.X.: Dietary and lifestyle factors associated withcolorectal cancer risk and interactions with microbiota: Fiber, redor processed meat and alcoholic drinks. Gastrointest. Tumors, 2016;3: 17–24
    Google Scholar
  • 49. Triantafyllou K., Chang C., Pimentel M.: Methanogens, methane andgastrointestinal motility. J. Neurogastroenterol. Motil., 2014; 20: 31–40
    Google Scholar
  • 50. Turnbaugh P.J., Ley R.E., Hamady M., Fraser-Liggett C.M., Knight R., Gordon J.I.: The human microbiome project. Nature, 2007; 449: 804–810
    Google Scholar
  • 51. Wang A.Y., Popov J., Pai N.: Fecal microbial transplant for the treatment of pediatric inflammatory bowel disease. Word J. Gastroenterol., 2016; 22: 10304–10315
    Google Scholar
  • 52. Wang L., Alammar N., Singh R., Nanavati J., Song Y., Chaudhary R., Mullin G.E.: Gut microbial dysbiosis in the irritable bowel syndrome: A systematic review and meta-analysis of case-control studies. J. Acad. Nutr. Diet., 2020; 120: 565–586
    Google Scholar
  • 53. Woese C.R., Kandler O., Wheelis M.L.: Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. USA, 1990; 87: 4576–4579
    Google Scholar
  • 54. Zhang H., DiBaise J.K., Zuccolo A., Kudrna D., Braidotti M., Yu Y., Parameswaran P., Crowell M.D., Wing R., Rittmann B.E., Krajmalnik- Brown R.: Human gut microbiota in obesity and after gastric bypass. Proc. Natl. Acad. Sci. USA, 2009; 106: 2365–2370
    Google Scholar

Full text

Skip to content