Archaea in and on the Human Body: Health Implications and Future Directions

1. Gill EE, Brinkman FS (2011) The proportional lack of archaeal pathogens: Do viruses/phages hold the key? Bioessays 33: 248–254. doi: 10.1002/bies.201000091 21328413

2. Cavicchioli R, Curmi PM, Saunders N, Thomas T (2003) Pathogenic archaea: do they exist? Bioessays 25: 1119–1128. 14579252

3. Walters WA, Caporaso JG, Lauber CL, Berg-Lyons D, Fierer N, et al. (2011) PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics 27: 1159–1161. doi: 10.1093/bioinformatics/btr087 21349862

4. Eckburg PB, Lepp PW, Relman DA (2003) Archaea and their potential role in human disease. Infect Immun 71: 591–596. 12540534

5. Horz HP, Conrads G (2010) The discussion goes on: What is the role of Euryarchaeota in humans? Archaea 2010: 967271. doi: 10.1155/2010/967271 21253553

6. Gaci N, Borrel G, Tottey W, O'Toole PW, Brugere JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20: 16062–16078. doi: 10.3748/wjg.v20.i43.16062 25473158

7. Dridi B, Raoult D, Drancourt M (2011) Archaea as emerging organisms in complex human microbiomes. Anaerobe 17: 56–63. doi: 10.1016/j.anaerobe.2011.03.001 21420503

8. Dridi B (2012) Laboratory tools for detection of archaea in humans. Clin Microbiol Infect 18: 825–833. doi: 10.1111/j.1469-0691.2012.03952.x 22897827

9. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59–65. doi: 10.1038/nature08821 20203603

10. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, et al. (2012) Human gut microbiome viewed across age and geography. Nature 486: 222–227. doi: 10.1038/nature11053 22699611

11. Oxley AP, Lanfranconi MP, Wurdemann D, Ott S, Schreiber S, et al. (2010) Halophilic archaea in the human intestinal mucosa. Environ Microbiol 12: 2398–2410. doi: 10.1111/j.1462-2920.2010.02212.x 20438582

12. Nottingham PM, Hungate RE (1968) M. J Bacteriol 96: 2178–2179. 4881707

13. Dridi B, Henry M, El Khechine A, Raoult D, Drancourt M (2009) High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLoS One 4: e7063. doi: 10.1371/journal.pone.0007063 19759898

14. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, et al. (2005) Diversity of the human intestinal microbial flora. Science 308: 1635–1638. 15831718

15. Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, et al. (2007) Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A 104: 10643–10648. 17563350

16. Miller TL, Wolin MJ, de Macario EC, Macario AJ (1982) Isolation of Methanobrevibacter smithii from human feces. Appl Environ Microbiol 43: 227–232. 6798932

17. Miller TL, Wolin MJ (1983) Stability of Methanobrevibacter smithii populations in the microbial flora excreted from the human large bowel. Appl Environ Microbiol 45: 317–318. 6824322

18. Hansen EE, Lozupone CA, Rey FE, Wu M, Guruge JL, et al. (2011) Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins. Proc Natl Acad Sci U S A 108 Suppl 1: 4599–4606. doi: 10.1073/pnas.1000071108 21317366

19. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, et al. (2014) Human genetics shape the gut microbiome. Cell 159: 789–799. doi: 10.1016/j.cell.2014.09.053 25417156

20. Fricke WF, Seedorf H, Henne A, Kruer M, Liesegang H, et al. (2006) The genome sequence of Methanosphaera stadtmanae reveals why this human intestinal archaeon is restricted to methanol and H2 for methane formation and ATP synthesis. J Bacteriol 188: 642–658. 16385054

21. Lurie-Weinberger MN, Peeri M, Tuller T, Gophna U (2012) Extensive Inter-Domain Lateral Gene Transfer in the Evolution of the Human Commensal Methanosphaera stadtmanae. Front Genet 3: 182. doi: 10.3389/fgene.2012.00182 23049536

22. Lurie-Weinberger MN, Peeri M, Gophna U (2012) Contribution of lateral gene transfer to the gene repertoire of a gut-adapted methanogen. Genomics 99: 52–58. doi: 10.1016/j.ygeno.2011.10.005 22056789

23. Bang C, Weidenbach K, Gutsmann T, Heine H, Schmitz RA (2014) The intestinal archaea Methanosphaera stadtmanae and Methanobrevibacter smithii activate human dendritic cells. PLoS One 9: e99411. doi: 10.1371/journal.pone.0099411 24915454

24. Blais Lecours P, Marsolais D, Cormier Y, Berberi M, Hache C, et al. (2014) Increased prevalence of Methanosphaera stadtmanae in inflammatory bowel diseases. PLoS One 9: e87734. doi: 10.1371/journal.pone.0087734 24498365

25. Leahy SC, Kelly WJ, Altermann E, Ronimus RS, Yeoman CJ, et al. (2010) The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One 5: e8926. doi: 10.1371/journal.pone.0008926 20126622

26. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027–1031. 17183312

27. Samuel BS, Gordon JI (2006) A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci U S A 103: 10011–10016. 16782812

28. Million M, Angelakis E, Maraninchi M, Henry M, Giorgi R, et al. (2013) Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int J Obes (Lond) 37: 1460–1466. doi: 10.1038/ijo.2013.20 23459324

29. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, et al. (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500: 541–546. doi: 10.1038/nature12506 23985870

30. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, et al. (2010) Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18: 190–195. doi: 10.1038/oby.2009.167 19498350

31. Pimentel M, Gunsalus RP, Rao SS, Zhang H (2012) Methanogens in Human Health and Disease. Am J Gastroenterol Suppl 6: 28–33.

32. Pimentel M, Lin HC, Enayati P, van den Burg B, Lee HR, et al. (2006) Methane, a gas produced by enteric bacteria, slows intestinal transit and augments small intestinal contractile activity. Am J Physiol Gastrointest Liver Physiol 290: G1089–1095. 16293652

33. Khelaifia S, Raoult D, Drancourt M (2013) A versatile medium for cultivating methanogenic archaea. PLoS One 8: e61563. doi: 10.1371/journal.pone.0061563 23613876

34. McKay LF, Eastwood MA, Brydon WG (1985) Methane excretion in man—a study of breath, flatus, and faeces. Gut 26: 69–74. 3965369

35. Borrel G, O'Toole PW, Harris HM, Peyret P, Brugere JF, et al. (2013) Phylogenomic data support a seventh order of Methylotrophic methanogens and provide insights into the evolution of Methanogenesis. Genome Biol Evol 5: 1769–1780. doi: 10.1093/gbe/evt128 23985970

36. Borrel G, Harris HM, Tottey W, Mihajlovski A, Parisot N, et al. (2012) Genome sequence of "Candidatus Methanomethylophilus alvus" Mx1201, a methanogenic archaeon from the human gut belonging to a seventh order of methanogens. J Bacteriol 194: 6944–6945. doi: 10.1128/JB.01867-12 23209209

37. Gorlas A, Robert C, Gimenez G, Drancourt M, Raoult D (2012) Complete genome sequence of Methanomassiliicoccus luminyensis, the largest genome of a human-associated Archaea species. J Bacteriol 194: 4745. doi: 10.1128/JB.00956-12 22887657

38. Brugere JF, Borrel G, Gaci N, Tottey W, O'Toole PW, et al. (2014) Archaebiotics: proposed therapeutic use of archaea to prevent trimethylaminuria and cardiovascular disease. Gut Microbes 5: 5–10. doi: 10.4161/gmic.26749 24247281

39. Wang Z, Klipfell E, Bennett BJ, Koeth R, Levison BS, et al. (2011) Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature 472: 57–63. doi: 10.1038/nature09922 21475195

40. Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, et al. (2013) Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 19: 576–585. doi: 10.1038/nm.3145 23563705

41. Brusa T, Conca R, Ferrara A, Ferrari A, Pecchioni A (1987) The presence of methanobacteria in human subgingival plaque. J Clin Periodontol 14: 470–471. 3308971

42. Ferrari A, Brusa T, Rutili A, Canzi E, Biavati B (1994) Isolation and characterization ofMethanobrevibacter oralis sp. nov. Current Microbiology 29: 7–12.

43. Kulik EM, Sandmeier H, Hinni K, Meyer J (2001) Identification of archaeal rDNA from subgingival dental plaque by PCR amplification and sequence analysis. FEMS Microbiol Lett 196: 129–133. 11267768

44. Belay N, Johnson R, Rajagopal BS, Conway de Macario E, Daniels L (1988) Methanogenic bacteria from human dental plaque. Appl Environ Microbiol 54: 600–603. 3355146

45. Robichaux M, Howell M, Boopathy R (2003) Methanogenic activity in human periodontal pocket. Curr Microbiol 46: 53–58. 12432465

46. Li CL, Liu DL, Jiang YT, Zhou YB, Zhang MZ, et al. (2009) Prevalence and molecular diversity of Archaea in subgingival pockets of periodontitis patients. Oral Microbiol Immunol 24: 343–346. doi: 10.1111/j.1399-302X.2009.00514.x 19572899

47. Horz HP, Seyfarth I, Conrads G (2012) McrA and 16S rRNA gene analysis suggests a novel lineage of Archaea phylogenetically affiliated with Thermoplasmatales in human subgingival plaque. Anaerobe 18: 373–377. doi: 10.1016/j.anaerobe.2012.04.006 22561061

48. Matarazzo F, Ribeiro AC, Feres M, Faveri M, Mayer MP (2011) Diversity and quantitative analysis of Archaea in aggressive periodontitis and periodontally healthy subjects. J Clin Periodontol 38: 621–627. doi: 10.1111/j.1600-051X.2011.01734.x 21539593

49. Faveri M, Goncalves LF, Feres M, Figueiredo LC, Gouveia LA, et al. (2011) Prevalence and microbiological diversity of Archaea in peri-implantitis subjects by 16S ribosomal RNA clonal analysis. J Periodontal Res 46: 338–344. doi: 10.1111/j.1600-0765.2011.01347.x 21338359

50. Nguyen-Hieu T, Khelaifia S, Aboudharam G, Drancourt M (2013) Methanogenic archaea in subgingival sites: a review. APMIS 121: 467–477. doi: 10.1111/apm.12015 23078250

51. Allers T, Mevarech M (2005) Archaeal genetics—the third way. Nat Rev Genet 6: 58–73. 15630422

52. Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2011) The antimicrobial resistance pattern of cultured human methanogens reflects the unique phylogenetic position of archaea. J Antimicrob Chemother 66: 2038–2044. doi: 10.1093/jac/dkr251 21680581

53. Lam WL, Doolittle WF (1989) Shuttle vectors for the archaebacterium Halobacterium volcanii. Proc Natl Acad Sci U S A 86: 5478–5482. 2748598

54. Hulcr J, Latimer AM, Henley JB, Rountree NR, Fierer N, et al. (2012) A jungle in there: bacteria in belly buttons are highly diverse, but predictable. PLoS One 7: e47712. doi: 10.1371/journal.pone.0047712 23144827

55. Oh J, Byrd AL, Deming C, Conlan S, Kong HH, et al. (2014) Biogeography and individuality shape function in the human skin metagenome. Nature 514: 59–64. doi: 10.1038/nature13786 25279917

56. Probst AJ, Auerbach AK, Moissl-Eichinger C (2013) Archaea on human skin. PLoS One 8: e65388. doi: 10.1371/journal.pone.0065388 23776475

57. Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, et al. (2011) Moving pictures of the human microbiome. Genome Biol 12: R50. doi: 10.1186/gb-2011-12-5-r50 21624126

58. Czarnowski D, Gorski J (1991) Sweat ammonia excretion during submaximal cycling exercise. J Appl Physiol (1985) 70: 371–374.

59. Sato K, Kang WH, Saga K, Sato KT (1989) Biology of sweat glands and their disorders. I. Normal sweat gland function. Journal of the American Academy of Dermatology 20: 537–563. 2654204

60. Miller TL, Wolin MJ (2001) Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylglutaryl-SCoA reductase inhibitors. J Dairy Sci 84: 1445–1448. 11417704

61. Bjorkhem-Bergman L, Lindh JD, Bergman P (2011) What is a relevant statin concentration in cell experiments claiming pleiotropic effects? Br J Clin Pharmacol 72: 164–165. doi: 10.1111/j.1365-2125.2011.03907.x 21223360

62. Blaser MJ, Falkow S (2009) What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 7: 887–894. doi: 10.1038/nrmicro2245 19898491

63. Spang A, Martijn J, Saw JH, Lind AE, Guy L, et al. (2013) Close Encounters of the Third Domain: The Emerging Genomic View of Archaeal Diversity and Evolution. Archaea 2013: 12.

64. Borrel G, Parisot N, Harris HM, Peyretaillade E, Gaci N, et al. (2014) Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine. BMC Genomics 15: 679. doi: 10.1186/1471-2164-15-679 25124552