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Zotero
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Ndiaye C, Bassene H, Diatta G, Daigne N, Parola P, Lagier JC, Sokhna C, Raolut D, 2020. The impact of daily soap use in rural areas of Senegal on respiratory infectious diseases, fevers and skin microbiota. Int J Infect Dis 96: 408–415.
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31.
Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, Raoult D, 2009. Ongoing revolution in bacteriology: Routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 49: 543–551.
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Morel A-S, Dubourg G, Prudent E, Edouard S, Gouriet F, Casalta J-P, Fenollar F, Drancourt M, Raoult D, 2015. Complementarity between targeted real-time specific PCR and conventional broad-range 16S rDNA PCR in the syndrome-driven diagnosis of infectious diseases. Eur J Clin Microbiol Infect Dis 34: 561–570.
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The Application of Culturomics to Explore African Skin Microbiota
Codou Ndiaye
Codou Ndiaye
UMR VITROME, Campus International IRD-UCAD de l’IRD de Hann, Dakar, Senegal;
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Hubert Bassene
hubert.bassene@ird.fr
Hubert Bassene
UMR VITROME, Campus International IRD-UCAD de l’IRD de Hann, Dakar, Senegal;
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Maxime Descartes Mbogning Fonkou
Maxime Descartes Mbogning Fonkou
Aix Marseille Université, IRD, AP-HM, Microbes Evolution Phylogeny and Infections (MEPHI), IHU-Méditerranée Infection, Marseille, France;
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Florence Fenollar
Florence Fenollar
Aix-Marseille Univ, IRD, AP-HM, SSA, IHU-Méditerranée Infection, UMR Vecteurs-Infections Tropicales et Méditerranéennes (VITROME), Marseille, France
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Jean Christophe Lagier
Jean Christophe Lagier
Aix Marseille Université, IRD, AP-HM, Microbes Evolution Phylogeny and Infections (MEPHI), IHU-Méditerranée Infection, Marseille, France;
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Didier Raoult
Didier Raoult
Aix Marseille Université, IRD, AP-HM, Microbes Evolution Phylogeny and Infections (MEPHI), IHU-Méditerranée Infection, Marseille, France;
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Cheikh Sokhna
Cheikh Sokhna
UMR VITROME, Campus International IRD-UCAD de l’IRD de Hann, Dakar, Senegal;
Aix-Marseille Univ, IRD, AP-HM, SSA, IHU-Méditerranée Infection, UMR Vecteurs-Infections Tropicales et Méditerranéennes (VITROME), Marseille, France
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Aix-Marseille Univ, IRD, AP-HM, SSA, IHU-Méditerranée Infection, UMR Vecteurs-Infections Tropicales et Méditerranéennes (VITROME), Marseille, France
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ABSTRACT.
Over the past 12 years, culturomics, a high-throughput culture method, has been developed, considerably widening the repertoire of known cultured bacteria. An exhaustive database, including a list of microbes isolated by culture from human skin, was recently established by performing a review of the literature. The aim of the present study was to use the culturomics approach to explore the African skin microbiota. Skin swabs from the palms of human hands were collected between January and December 2016 from healthy subjects from the villages of Dielmo and Ndiop in rural Senegal. Three culture media were selected for the isolation of bacteria in aerobic conditions. Bacterial colonies were subjected to matrix-assisted laser desorption ionization–time of flight mass spectroscopy and the 16 S rRNA gene was sequenced for unidentified colonies. A total of 176 bacterial species were isolated. This increased the repertoire of bacterial species on the skin by 14.0%, by adding 71 bacteria, including seven new species. The culturomics approach characterizing microbial diversity has significantly changed our view of the skin microbiota, raising many important questions about the host-microorganism relationship and its relevance to skin diseases. In particular, the difference between the palm microbiota of these African populations (composed mainly of the genera Staphylococcus, Arthrobacter, Bacillus, and Microbacterium) and that of Western populations, whose main genera are Staphylococcus, Propionibacterium, Micrococcus, Corynebacterium, Enhydrobacter, and Streptococcus. This study demonstrates the need to continue to explore the skin microbiome using the culturomics approach
- Supplemental Materials (PDF 844.59 KB)
Author Notes
Authors’ contributions: Conceptualization: D. Raoult. Data curation: C. Ndiaye, H. Bassene, M. D. M. Fonkou. Formal analysis: C. Ndiaye, H. Bassene. Funding acquisition: D. Raoult. Investigation: C. Ndiaye, H. Bassene. Methodology: H. Bassene, J. C. Lagier, C. Sokhna. Project administration: H. Bassene. Software: C. Ndiaye, M. D. M. Fonkou. Supervision: C. Ndiaye, H. Bassene. Validation: D. Raoult. Writing—original draft: C. Ndiaye, H. Bassene, M. D. M. Fonkou. Writing—review and editing: H. Bassene, J. C. Lagier, F. Fenollar, C. Sokhna, D. Raoult.
Financial support: This work has benefited from support from the French State, managed by the
Disclosure: Before inclusion in the study, written informed consent was required from all adult participants (≥18 years) and from parents or legal guardians of minors (<18 years). An information document clearly explaining the risks and benefits associated with participation in the study was given to each patient. This document set out the reasons and purpose of the sampling, in the presence of a parent/legal tutor. The consent form stipulated that samples would not be used in the future in other studies not related to the present study without prior agreement from the participant and the Senegalese Ethics Committee. The study was approved by the Senegalese Ethics Committee (No. 53/MSAS/DPRS/CNERS of 31 March 2015), and consent was obtained from each individual.
Current contact information: Codou Ndiaye, Maxime Descartes Mbogning Fonkou, Jean Christophe Lagier, and Didier Raoult, IRD, AP-HM, Microbes Evolution Phylogeny and Infections (MEPHI), IHU-Mediterranée Infection, Aix Marseille Université, Marseille, France, E-mails: codoundiaye134@yahoo.fr, dmbogning15@gmail.com, jclagier@yahoo.fr, and didier.raoult@gmail.com. Hubert Bassene, EMR MINES, Campus Commun UCAD-IRD de Hann, IRD, Dakar 1386, Senegal, E-mail: hubert.bassene@ird.fr. Florence Fenollar, IHU-Méditerranée Infection, 19-21 Boulevard Jean Moulin, 13005 Marseille, France; Campus Santé Timone, Aix Marseille University, AP-HM, SSA, RITMES, 13005 Marseille, France, E-mail: florence.fenollar@univ-amu.fr. Cheikh Sokhna, EMR MINES, Campus Commun UCAD-IRD de Hann, IRD, Dakar 1386, Senegal; Campus Santé Timone, Aix Marseille University, AP-HM, SSA, RITMES, 13005 Marseille, France, E-mail: cheikh.sokhna@ird.fr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Zeeuwen PL, Kleerebezem M, Timmerman HM, Schalkwijk J, 2013. Microbiome and skin diseases. Curr Opin Allergy Clin Immunol 13: 514–520.
-
3.
Tomic-Canic M, Perez-Perez GI, Blumenberg M, 2014. Cutaneous microbiome studies in the times of affordable sequencing. J Dermatol Sci 75: 82–87.
-
4.
Grice EA, Segre JA, 2012. The human microbiome: Our second genome. Annu Rev Genomics Hum Genet 13: 151–170.
-
5.
Scott E, Bloomfield SF, 1990. The survival and transfer of microbial contamination via cloths, hands and utensils. J Appl Bacteriol 68: 271–278.
-
6.
Lax S, et al., 2014. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345: 1048–1052.
-
7.
Leyden JJ, Mcginley KJ, Nordstrom KM, Webster GF, 1987. Skin microflora. J Invest Dermatol 88: S65–S72.
-
8.
Proctor LM, 2011. The human microbiome project in 2011 and beyond. Cell Host Microbe 10: 287–291.
-
9.
Fleming E, et al., 2021. Cultivation of common bacterial species and strains from human skin, oral, and gut microbiota. BMC Microbiol 21: 278.
-
10.
Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA, 2005. Diversity of the human intestinal microbial flora. Science 308: 1635–1638.
-
11.
O’Hara AM, Shanahan F, 2006. The gut flora as a forgotten organ. EMBO Rep 7: 688–693.
-
12.
Kelly D, Conway S, Aminov R, 2005. Commensal gut bacteria: Mechanisms of immune modulation. Trends Immunol 26: 326–333.
-
13.
Peterson J, et al., 2009. The NIH human microbiome project. Genome Res 19: 2317–2323.
-
14.
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R, 2009. Bacterial community variation in human body habitats across space and time. Science 326: 1694–1697.
-
15.
Gao Z, Tseng C-h, Pei Z, Blaser MJ, 2007. Molecular analysis of human forearm superficial skin bacterial biota. Proc Natl Acad Sci USA 104: 2927–2932.
-
16.
De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P, 2010. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107: 14691–14696.
-
17.
Grice EA, Kong HH, Renaud G, Young AC, Bouffard GG, Blakesley RW, Wolfsberg TG, Turner ML, Segre JA; NISC Comparative Sequencing Program, 2008. A diversity profile of the human skin microbiota. Genome Res 18: 1043–1050.
-
18.
Perez GIP, Gao Z, Jourdain R, Ramirez J, Gany F, Clavaud C, Demaude J, Breton L, Breton L, 2016. Body site is a more determinant factor than human population diversity in the healthy skin microbiome. PLoS One 11: e0151990.
-
19.
Kong HH, et al., 2012. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22: 850–859.
-
20.
Blaser MJ, Falkow S, 2009. What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 7: 887–894.
-
21.
Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI, 2008. Worlds within worlds: Evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6: 776–788.
-
22.
Pei Z, Bini EJ, Yang L, Zhou M, Francois F, Blaser MJ, 2004. Bacterial biota in the human distal esophagus. Proc Natl Acad Sci USA 101: 4250–4255.
-
23.
Kaeberlein T, Lewis K, Epstein SS, 2002. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296: 1127–1129.
-
24.
Lagier J-C, Dubourg G, Million M, Cadoret F, Bilen M, Fenollar F, Levasseur A, Rolain J-M, Fournier P-E, Raoult D, 2018. Culturing the human microbiota and culturomics. Nat Rev Microbiol 16: 540–550.
-
25.
Lagier J-C, Hugon P, Khelaifia S, Fournier P-E, La Scola B, Raoult D, 2015. The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin Microbiol Rev 28: 237–264.
-
26.
Ramadan M, Solyman S, Taha M, Hanora A, 2016. Preliminary characterization of human skin microbiome in healthy Egyptian individuals. Cell Mol Biol 62: 21–27.
-
27.
Ndiaye C, Bassene H, Lagier JC, Raoult D, Sokhna C, 2018. Asymptomatic carriage of Streptococcus pneumoniae detected by qPCR on the palm of hands of populations in rural Senegal. PLoS Negl Trop Dis 12: e0006945.
-
28.
Ndiaye C, Bassene H, Diatta G, Daigne N, Parola P, Lagier JC, Sokhna C, Raolut D, 2020. The impact of daily soap use in rural areas of Senegal on respiratory infectious diseases, fevers and skin microbiota. Int J Infect Dis 96: 408–415.
-
29.
Lagier JC, et al., 2012. Microbial culturomics: Paradigm shift in the human gut microbiome study. Clin Microbiol Infect 18: 1185–1193.
-
30.
Dione N, Khelaifia S, La Scola B, Lagier J, Raoult D, 2016. A quasi-universal medium to break the aerobic/anaerobic bacterial culture dichotomy in clinical microbiology. Clin Microbiol Infect 22: 53–58.
-
31.
Seng P, Drancourt M, Gouriet F, La Scola B, Fournier PE, Rolain JM, Raoult D, 2009. Ongoing revolution in bacteriology: Routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clin Infect Dis 49: 543–551.
-
32.
Morel A-S, Dubourg G, Prudent E, Edouard S, Gouriet F, Casalta J-P, Fenollar F, Drancourt M, Raoult D, 2015. Complementarity between targeted real-time specific PCR and conventional broad-range 16S rDNA PCR in the syndrome-driven diagnosis of infectious diseases. Eur J Clin Microbiol Infect Dis 34: 561–570.
-
33.
Brown RL, Sequeira RP, Clarke TB, 2017. The microbiota protects against respiratory infection via GM-CSF signaling. Nat Commun 8: 1512.
-
34.
Stackebrandt E, 2006. Taxonomic parameters revisited: Tarnished gold standards. Microbiol Today 33: 152–155.
-
35.
Ramasamy D, Mishra AK, Lagier J-C, Padhmanabhan R, Rossi M, Sentausa E, Raoult D, Fournier P-E, 2014. A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 64: 384–391.
-
36.
Ndiaye C, Bassène H, Cadoret F, Raoult D, Lagier JC, Sokhna C, 2018. ‘Citricoccus massiliensis’ sp. nov., a new bacterial species isolated from human skin by culturomics. New Microbes New Infect 23: 83–85.
-
37.
Ndiaye C, Lo CI, Bassene H, 2019. Lysinibacillus timonensis sp. nov., Microbacterium timonense sp. nov., and Erwinia mediterraneensis sp. nov., three new species isolated from the human skin. New Microbes New Infect 31: 100579.
-
38.
Ndiaye C, Fall NS, Kuete E, Lo CI, Raoult D, Sokhna C, Lagier JC, 2019. Corynebacterium senegalense sp. nov. and Arthrobacter senegalensis sp. nov., two new Actinobacteria isolated from skin swab from the palm of hand. New Microbes New Infect 31: 100583.
-
39.
Bilen M, Dufour J-C, Lagier J-C, Cadoret F, Daoud Z, Dubourg G, Raoult D, 2018. The contribution of culturomics to the repertoire of isolated human bacterial and archaeal species. Microbiome 6: 94.
-
40.
Lagier J-C, et al., 2016. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol 1: 16203.
-
41.
Morand A, Cornu F, Cufour J-C, Tsimaratos M, Lagier J-C, Raoult D, 2019. Human bacterial repertoire of the urinary tract: A potential paradigm shift. J Clin Microbiol 57: e00675-18.
-
42.
Diop K, Dufour J-C, Levasseur A, Fenollar F, 2019. Exhaustive repertoire of human vaginal microbiota. Hum Microbiome J 11: 100051.
-
43.
Togo A, Dufour J-C, Lagier J-C, Dubourg G, Raoult D, Million D, 2019. Repertoire of human breast and milk microbiota: A systematic review. Future Microbiol 14: 623–641.
-
44.
Mbogning Fonkou M, 2018. Exploration du microbiote respiratoire humain. PhD Thesis, Aix-Marseille Université.
-
45.
Lira-Junior R, Boström E, 2018. Oral-gut connection: One step closer to an integrated view of the gastrointestinal tract? Mucosal Immunol 11: 316.
-
46.
Zeeuwen PL, et al., 2012. Microbiome dynamics of human epidermis following skin barrier disruption. Genome Biol 13: R101.
-
47.
Schloss PD, 2014. Microbiology: An integrated view of the skin microbiome. Nature 514: 44–45.
-
48.
Kong HH, Segre JA, 2012. Skin microbiome: Looking back to move forward. J Invest Dermatol 132: 933–939.
-
49.
Dreno B, Araviiskaia E, Berardesca E, Gontijo G, Sanchez Viera M, Xiang LF, Martin R, Bieber T, 2016. Microbiome in healthy skin, update for dermatologists. J Eur Acad Dermatol Venereol 30: 2038–2047.
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