Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 12/2017

01-12-2017 | Original Article

Methanobrevibacter smithii, a methanogen consistently colonising the newborn stomach

Authors: G. Grine, M. A. Boualam, M. Drancourt

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 12/2017

Login to get access

Abstract

Methanobrevibacter smithii is the main human methanogen almost always found in the digestive tract of adults. Yet, the age at which M. smithii establishes itself as part of the developing intestinal microflora remains unknown. In order to gain insight into this, we developed a polyphasic approach, including microscopic observation by fluorescence in situ hybridisation, polymerase chain reaction (PCR) sequencing detection, identification and culture, to isolate and genotype M. smithii in one-day-old newborns’ gastric juice specimens. In the presence of negative controls, 50/50 (100%) prospectively analysed newborn gastric juice specimens were PCR-positive for methanogens, all identified as M. smithii by sequencing. We succeeded in cultivating M. smithii in 35/50 (70%) newborn gastric juice specimens, while 15/50 specimens remained sterile. Further, M. smithii was observed by direct microscopic investigation using fluorescence in situ hybridisation. Multispacer sequence typing found one of seven different genotypes per specimen, these genotypes having all been previously described in adult human stools. Methanobrevibacter smithii is an early inhabitant of the human stomach, colonising the gastric mucosa just after birth, and the mother’s gut microbiota is a probable source of colonisation.
Literature
1.
go back to reference Dridi B, Henry M, El Khéchine 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(9):e7063 Dridi B, Henry M, El Khéchine 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(9):e7063
2.
go back to reference Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62(Pt 8):1902–1907 Dridi B, Fardeau ML, Ollivier B, Raoult D, Drancourt M (2012) Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62(Pt 8):1902–1907
3.
go back to reference Khelaifia S, Raoult D, Drancourt M (2013) A versatile medium for cultivating methanogenic archaea. PLoS One 8(4):e61563 Khelaifia S, Raoult D, Drancourt M (2013) A versatile medium for cultivating methanogenic archaea. PLoS One 8(4):e61563
4.
go back to reference Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, Fulton R, Latreille P, Kim K, Wilson RK, Gordon JI (2007) Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A 104(25):10643–10648 Samuel BS, Hansen EE, Manchester JK, Coutinho PM, Henrissat B, Fulton R, Latreille P, Kim K, Wilson RK, Gordon JI (2007) Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut. Proc Natl Acad Sci U S A 104(25):10643–10648
5.
go back to reference Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177 Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5(7):e177
6.
go back to reference Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108(Suppl 1):4578–4585 Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE (2011) Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108(Suppl 1):4578–4585
7.
go back to reference Mihajlovski A, Doré J, Levenez F, Alric M, Brugère JF (2010) Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity. Environ Microbiol Rep 2(2):272–280 Mihajlovski A, Doré J, Levenez F, Alric M, Brugère JF (2010) Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity. Environ Microbiol Rep 2(2):272–280
8.
go back to reference Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20(43):16062–16078 Gaci N, Borrel G, Tottey W, O’Toole PW, Brugère JF (2014) Archaea and the human gut: new beginning of an old story. World J Gastroenterol 20(43):16062–16078
9.
go back to reference Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao JZ, Abe F, Osawa R (2016) Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol 16:90 Odamaki T, Kato K, Sugahara H, Hashikura N, Takahashi S, Xiao JZ, Abe F, Osawa R (2016) Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol 16:90
10.
go back to reference Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol 3B. Academic Press, Cambridge, pp 117–132 Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. In: Norris JR, Ribbons DW (eds) Methods in microbiology, vol 3B. Academic Press, Cambridge, pp 117–132
11.
go back to reference Hungate RE, Macy J (1973) The roll-tube method for cultivation of strict anaerobes. Bulletins from the Ecological Research Committee/NFR, No. 17, Modern Methods in the Study of Microbial Ecology. Oikos Editorial Office, pp 123–126 Hungate RE, Macy J (1973) The roll-tube method for cultivation of strict anaerobes. Bulletins from the Ecological Research Committee/NFR, No. 17, Modern Methods in the Study of Microbial Ecology. Oikos Editorial Office, pp 123–126
12.
go back to reference Khelaifia S, Lagier JC, Nkamga VD, Guilhot E, Drancourt M, Raoult D (2016) Aerobic culture of methanogenic archaea without an external source of hydrogen. Eur J Clin Microbiol Infect Dis 35(6):985–991 Khelaifia S, Lagier JC, Nkamga VD, Guilhot E, Drancourt M, Raoult D (2016) Aerobic culture of methanogenic archaea without an external source of hydrogen. Eur J Clin Microbiol Infect Dis 35(6):985–991
14.
go back to reference Nkamga VD, Huynh HT, Aboudharam G, Ruimy R, Drancourt M (2015) Diversity of human-associated Methanobrevibacter smithii isolates revealed by multispacer sequence typing. Curr Microbiol 70(6):810–815 Nkamga VD, Huynh HT, Aboudharam G, Ruimy R, Drancourt M (2015) Diversity of human-associated Methanobrevibacter smithii isolates revealed by multispacer sequence typing. Curr Microbiol 70(6):810–815
15.
go back to reference Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60(4):1232–1240 Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60(4):1232–1240
16.
go back to reference Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148(Pt 11):3521–3530 Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148(Pt 11):3521–3530
17.
go back to reference Sondheimer JM, Clark DA, Gervaise EP (1985) Continuous gastric pH measurement in young and older healthy preterm infants receiving formula and clear liquid feedings. J Pediatr Gastroenterol Nutr 4(3):352–355 Sondheimer JM, Clark DA, Gervaise EP (1985) Continuous gastric pH measurement in young and older healthy preterm infants receiving formula and clear liquid feedings. J Pediatr Gastroenterol Nutr 4(3):352–355
18.
go back to reference Mason S (1962) Some aspects of gastric function in the newborn. Arch Dis Child 37:387–391 Mason S (1962) Some aspects of gastric function in the newborn. Arch Dis Child 37:387–391
19.
go back to reference Belay N, Mukhopadhyay B, Conway de Macario E, Galask R, Daniels L (1990) Methanogenic bacteria in human vaginal samples. J Clin Microbiol 28(7):1666–1668 Belay N, Mukhopadhyay B, Conway de Macario E, Galask R, Daniels L (1990) Methanogenic bacteria in human vaginal samples. J Clin Microbiol 28(7):1666–1668
20.
go back to reference Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17(5):690–703 Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, Li Y, Xia Y, Xie H, Zhong H, Khan MT, Zhang J, Li J, Xiao L, Al-Aama J, Zhang D, Lee YS, Kotowska D, Colding C, Tremaroli V, Yin Y, Bergman S, Xu X, Madsen L, Kristiansen K, Dahlgren J, Wang J (2015) Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17(5):690–703
21.
go back to reference Jiménez E, de Andrés J, Manrique M, Pareja-Tobes P, Tobes R, Martínez-Blanch JF, Codoñer FM, Ramón D, Fernández L, Rodríguez JM (2015) Metagenomic analysis of milk of healthy and mastitis-suffering women. J Hum Lact 31(3):406–415 Jiménez E, de Andrés J, Manrique M, Pareja-Tobes P, Tobes R, Martínez-Blanch JF, Codoñer FM, Ramón D, Fernández L, Rodríguez JM (2015) Metagenomic analysis of milk of healthy and mastitis-suffering women. J Hum Lact 31(3):406–415
23.
go back to reference Hansen EE, Lozupone CA, Rey FE, Wu M, Guruge JL, Narra A, Goodfellow J, Zaneveld JR, McDonald DT, Goodrich JA, Heath AC, Knight R, Gordon JI (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 Hansen EE, Lozupone CA, Rey FE, Wu M, Guruge JL, Narra A, Goodfellow J, Zaneveld JR, McDonald DT, Goodrich JA, Heath AC, Knight R, Gordon JI (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
24.
go back to reference Vallès Y, Gosalbes MJ, de Vries LE, Abellán JJ, Francino MP (2012) Metagenomics and development of the gut microbiota in infants. Clin Microbiol Infect 18(Suppl 4):21–26 Vallès Y, Gosalbes MJ, de Vries LE, Abellán JJ, Francino MP (2012) Metagenomics and development of the gut microbiota in infants. Clin Microbiol Infect 18(Suppl 4):21–26
Metadata
Title
Methanobrevibacter smithii, a methanogen consistently colonising the newborn stomach
Authors
G. Grine
M. A. Boualam
M. Drancourt
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 12/2017
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-017-3084-7

Other articles of this Issue 12/2017

European Journal of Clinical Microbiology & Infectious Diseases 12/2017 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.