Abstract
Over the past decade, new culture methods coupled to genome and metagenome sequencing have enabled the number of isolated bacterial species with standing in nomenclature to rise to more than 15,000 whereas it was only 1791 in 1980. ‘Culturomics’, a new approach based on the diversification of culture conditions, has enabled the isolation of more than 1000 distinct human-associated bacterial species since 2012, including 247 new species. This strategy was demonstrated to be complementary to metagenome sequencing for the exhaustive study of the human microbiota and its roles in health and diseases. However, by identifying a large number of new bacterial species in a short time, culturomics has highlighted a need for taxonomic approaches adapted to clinical microbiology that would include the use of modern and reproducible tools, including high throughput genomic and proteomic analyses. Herein, we review the development of culturomics and genomics in the clinical microbiology field and their impact on bacterial taxonomy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andersson AF, Lindberg M, Jakobsson H et al (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 3:e2836. doi:10.1371/journal.pone.0002836
Antony R, Krishnan KP, Laluraj CM et al (2012) Diversity and physiology of culturable bacteria associated with a coastal Antarctic ice core. Microbiol Res 167:372–380. doi:10.1016/j.micres.2012.03.003
Armougom F, Henry M, Vialettes B et al (2009) Monitoring bacterial community of human gut microbiota reveals an increase in lactobacillus in obese patients and methanogens in anorexic patients. PLoS ONE 4:e7125. doi:10.1371/journal.pone.0007125
Azevedo H, Lopes F, Silla P, Hungria M (2015) A database for the taxonomic and phylogenetic identification of the genus Bradyrhizobium using multilocus sequence analysis. BMC Genom 16(Suppl 5):S10. doi:10.1186/1471-2164-16-S5-S10
Bomar L, Maltz M, Colston S, Graf J (2011) Directed culturing of microorganisms using metatranscriptomics. mBio 2:e00012–11. doi:10.1128/mBio.00012-11
Brenner DJ, Fanning GR, Rake AV, Johnson KE (1969) Batch procedure for thermal elution of DNA from hydroxyapatite. Anal Biochem 28:447–459. doi:10.1016/0003-2697(69)90199-7
Camelo-Castillo A, Benítez-Páez A, Belda-Ferre P et al (2014) Streptococcus dentisani sp. nov., a novel member of the mitis group. Int J Syst Evol Microbiol 64:60–65. doi:10.1099/ijs.0.054098-0
Claesson MJ, Wang Q, O’Sullivan O et al (2010) Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Res 38:gkq873–e200. doi:10.1093/nar/gkq873
Collins MD (2004) Corynebacterium caspium sp. nov., from a Caspian seal (Phoca caspica). Int J Syst Evol Microbiol 54:925–928. doi:10.1099/ijs.0.02950-0
De Hertogh G, Aerssens J, De Hoogt R et al (2006) Validation of 16S rDNA sequencing in microdissected bowel biopsies from Crohn’s disease patients to assess bacterial flora diversity. J Pathol 209:532–539. doi:10.1002/path.2006
Diop A, Khelaifia S, Armstrong N et al (2016) Microbial culturomics unravels the halophilic microbiota repertoire of table salt: description of Gracilibacillus massiliensis sp. nov. Microb Ecol Health Dis 27:32049. doi:10.3402/mehd.v27.32049
Drancourt M, Raoult D (2007) Cost-effectiveness of blood agar for isolation of mycobacteria. PLOS Negl Trop Dis 1:e83. doi:10.1371/journal.pntd.0000083
Drancourt M, Carrieri P, Gévaudan MJ, Raoult D (2003) Blood agar and mycobacterium tuberculosis: the end of a dogma. J Clin Microbiol 41:1710–1711. doi:10.1128/JCM.41.4.1710-1711.2003
Finegold SM, Attebery HR, Sutter VL (1974) Effect of diet on human fecal flora: comparison of Japanese and American diets1′2. Am J Clin Nutr 27(12):1456–1469
Fleischmann RD, Adams MD, White O et al (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512
Fournier PE, Drancourt M (2015) New microbes new infections promotes modern prokaryotic taxonomy: a new section “TaxonoGenomics: new genomes of microorganisms in humans”. New Microbes New Infect 7:48–49. doi:10.1016/j.nmni.2015.06.001
Fournier PE, Lagier J-C, Dubourg G, Raoult D (2015) From culturomics to taxonomogenomics: a need to change the taxonomy of prokaryotes in clinical microbiology. Anaerobe 36:73–78. doi:10.1016/j.anaerobe.2015.10.011
Fournier PE, Raoult D, Dancourt M (2016) New species announcements: a new format to prompt the description of new human microbial species. New Microbes New Infect 15:136–137. doi:10.1016/j.nmni.2016.04.006
Fox GE, Wisotzkey JD, Jurtshuk P Jr (1992) How close is close: 16S rRNA sequence identity may not be sufficient to guarantee species identity. Int J Syst Evol Microbiol 42:166–170. doi:10.1099/00207713-42-1-166
Glaeser SP, Kämpfer P (2015) Multilocus sequence analysis (MLSA) in prokaryotic taxonomy. Syst Appl Microbiol 38:237–245. doi:10.1016/j.syapm.2015.03.007
Goodman AL, Kallstrom G, Faith JJ et al (2011) Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice. Proc Natl Acad Sci USA 108:6252–6257. doi:10.1073/pnas.1102938108
Goris J, Konstantinidis KT, Klappenbach JA et al (2007) DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91. doi:10.1099/ijs.0.64483-0
Greub G (2016) Culturomics: a new approach to study the human microbiome. Clin Microbiol Infect 18:1157–1159. doi:10.1111/1469-0691.12032
Guijarro JA, Cascales D, García-Torrico AI et al (2015) Temperature-dependent expression of virulence genes in fish-pathogenic bacteria. Front Microbiol 6:700. doi:10.3389/fmicb.2015.00700
Hiergeist A, Gläsner J, Reischl U, Gessner A (2015) Analyses of intestinal microbiota: culture versus sequencing. ILAR J 56:228–240. doi:10.1093/ilar/ilv017
Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774. doi:10.1007/BF00039173
Hugon P, Lagier J-C, Colson P et al (2016) Repertoire of human gut microbes. Microb Pathog. doi:10.1016/j.micpath.2016.06.020
Huson DH, Steel M (2004) Phylogenetic trees based on gene content. Bioinformatics 20:2044–2049. doi:10.1093/bioinformatics/bth198
Jiang X, Doyle MP (2002) Optimizing enrichment culture conditions for detecting helicobacter pylori in foods. J Food Prot 65(12):1949–1954
Johnson JL (1973) Use of nucleic-acid homologies in the taxonomy of anaerobic bacteria. Int J Syst Evolutionary Microbiol 23:308–315
Johnson JL (1991) DNA reassociation experiments. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 21–44
Karlsson F, Tremaroli V, Nielsen J, Bäckhed F (2013) Assessing the human gut microbiota in metabolic diseases. Diabetes 62:3341–3349. doi:10.2337/db13-0844
Kau AL, Ahern PP, Griffin NW et al (2011) Human nutrition, the gut microbiome and the immune system. Nature 474:327–336. doi:10.1038/nature10213
Kim BS, Kim JN, Cerniglia CE (2011) In vitro culture conditions for maintaining a complex population of human gastrointestinal tract microbiota. J Biomed Biotechnol. doi:10.1155/2011/838040
Kim M, Oh H-S, Park S-C, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351. doi:10.1099/ijs.0.059774-0
Kim M, Park SC, Baek I et al (2015) Large-scale evaluation of experimentally determined DNA G+C contents with whole genome sequences of prokaryotes. Syst Appl Microbiol 38:79–83. doi:10.1016/j.syapm.2014.11.008
Lagier JC, Armougom F, Million M et al (2012) Microbial culturomics: paradigm shift in the human gut microbiome study. Clin Microbiol Infect 18:1185–1193. doi:10.1111/1469-0691.12023
Lagier J-C, Elkarkouri K, Rivet R et al (2013) Non contiguous-finished genome sequence and description of Senegalemassilia anaerobia gen. nov., sp. nov. Stand Genom Sci 7:343–356. doi:10.4056/sigs.3246665
Lagier J-C, Hugon P, Khelaifia S et al (2015a) The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin Microbiol Rev 28:237–264. doi:10.1128/CMR.00014-14
Lagier J-C, Edouard S, Pagnier I et al (2015b) Current and past strategies for bacterial culture in clinical microbiology. Clin Microbiol Rev 28:208–236. doi:10.1128/CMR.00110-14
Lagier J-C, Khelaifia S, Alou MT et al (2016) Culture of previously uncultured members of the human gut microbiota by culturomics. Nat Microbiol 1:16203. doi:10.1038/nmicrobiol.2016.203
Larsen N, Vogensen FK, van den Berg FWJ et al (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5:e9085. doi:10.1371/journal.pone.0009085
Lau JT, Whelan FJ, Herath I et al (2016) Capturing the diversity of the human gut microbiota through culture-enriched molecular profiling. Genome Med 8:1635. doi:10.1186/s13073-016-0327-7
LeChevallier MW, Cameron SC, McFeters GA (1983) New medium for improved recovery of coliform bacteria from drinking water. Appl Environ Microbiol 45:484–492
Lee I, Ouk Kim Y, Chun J, Park S-C (2016) OrthoANI: an improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol 66:1100–1103. doi:10.1099/ijsem.0.000760
Liu L, Salam N, Jiao J-Y et al (2016) Diversity of culturable thermophilic actinobacteria in hot springs in tengchong, China and studies of their biosynthetic gene profiles. Microb Ecol 72:150–162. doi:10.1007/s00248-016-0756-2
Löffler FE, Yan J, Ritalahti KM et al (2013) Dehalococcoides mccartyi gen. nov., sp. nov., obligately organohalide-respiring anaerobic bacteria relevant to halogen cycling and bioremediation, belong to a novel bacterial class, Dehalococcoidia classis nov., order Dehalococcoidales ord. nov. and family Dehalococcoidaceae fam. nov., within the phylum Chloroflexi. Int J Syst Evol Microbiol 63:625–635. doi:10.1099/ijs.0.034926-0
Ludwig W, Klenk H-P (2001) Overview: a phylogenetic backbone and taxonomic framework for procaryotic systematics. Bergey’s manual® of systematic bacteriology. Springer, New York, pp 49–65
Maiden M, Bygraves JA, Feil E et al (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA 95:3140–3145. doi:10.1073/pnas.95.6.3140
Marchesi JR, Ravel J (2015) The vocabulary of microbiome research: a proposal. Microbiome. doi:10.1186/s40168-015-0094-5
Minnikin DE, Alshamaony L, GOODFELLOW M (1975) Differentiation of mycobacterium, nocardia, and related taxa by thin-layer chromatographic analysis of whole-organism methanolysates. Microbiology 88:200–204. doi:10.1099/00221287-88-1-200
Overmann J (2015) Green sulfur bacteria. Wiley, Chichester
Overmann J, Garcia-Pichel F (2013) The Phototrophic Way of Life. The Prokaryotes. Springer, Heidelberg, pp 203–257
Ramasamy D, Mishra AK, Lagier J-C et al (2014) A polyphasic strategy incorporating genomic data for the taxonomic description of novel bacterial species. Int J Syst Evol Microbiol 64:384–391. doi:10.1099/ijs.0.057091-0
Raoult D (2016) Human gut microbiota: repertoire and variations. Front Cell Infect Microbiol. doi:10.3389/fcimb.2012.00136/abstract
Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci USA 106:19126–19131. doi:10.1073/pnas.0906412106
Rossello-Mora R, Trujillo ME, Sutcliffe IC (2017) Introducing a digital protologue: a timely move towards a database-driven systematic of archaea and bacteria. Antonie Van Leeuwenhoek 110:455–456. doi:10.1007/s10482-017-0841-7
Rossi-Tamisier M, Benamar S, Raoult D, Fournier PE (2015) Cautionary tale of using 16S rRNA gene sequence similarity values in identification of human-associated bacterial species. Int J Syst Evol Microbiol 65:1929–1934. doi:10.1099/ijs.0.000161
Sankar SA, Lagier J-C, Pontarotti P et al (2015) The human gut microbiome, a taxonomic conundrum. Syst Appl Microbiol 38:276–286. doi:10.1016/j.syapm.2015.03.004
Schleifer KH (2009) Classification of bacteria and archaea: past, present and future. Syst Appl Microbiol 32:533–542. doi:10.1016/j.syapm.2009.09.002
Schmeisser C, Stöckigt C, Raasch C et al (2003) Metagenome survey of biofilms in drinking-water networks. Appl Environ Microbiol 69:7298–7309. doi:10.1128/AEM.69.12.7298-7309.2003
Sentausa E, Fournier PE (2013) Advantages and limitations of genomics in prokaryotic taxonomy. Clin Microbiol Infect 19:790–795. doi:10.1111/1469-0691.12181
Sibley CD, Grinwis ME, Field TR et al (2011) Culture enriched molecular profiling of the cystic fibrosis airway microbiome. PLoS ONE 6:e22702. doi:10.1371/journal.pone.0022702
Siggers RH, Siggers J, Boye M et al (2008) Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138:1437–1444
Simner PJ, Doerr KA, Steinmetz LK, Wengenack NL (2016) Mycobacterium and aerobic actinomycete culture: are two medium types and extended incubation times necessary? J Clin Microbiol 54:1089–1093. doi:10.1128/JCM.02838-15
Singh S, Eldin C, Kowalczewska M, Raoult D (2013) Axenic culture of fastidious and intracellular bacteria. Trends Microbiol 21:92–99. doi:10.1016/j.tim.2012.10.007
Skerman VBD, McGowan V, Sneath PHA (eds) (1989) Approved lists of bacterial names (Amended). ASM Press, Washington (DC)
Snel B, Bork P, Huynen MA (1999) Genome phylogeny based on gene content. Nat Genet 21:108–110. doi:10.1038/5052
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152
Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 44:846–849. doi:10.1099/00207713-44-4-846
Subramanyam B, Sivaramakrishnan GN, Dusthackeer A et al (2012) Phage lysin as a substitute for antibiotics to detect Mycobacterium tuberculosis from sputum samples with the BACTEC MGIT 960 system. Clin Microbiol Infect 18:497–501. doi:10.1111/j.1469-0691.2011.03601.x
Sutcliffe IC (2015) Challenging the anthropocentric emphasis on phenotypic testing in prokaryotic species descriptions: rip it up and start again. Front Genet 6:218. doi:10.3389/fgene.2015.00218
Tatusov RL, Natale DA, Garkavtsev IV et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28. doi:10.1093/nar/29.1.22
Tidjani Alou M, Khelaifia S, Michelle C et al (2016) Anaerococcus rubiinfantis sp. nov., isolated from the gut microbiota of a Senegalese infant with severe acute malnutrition. Anaerobe 40:85–94. doi:10.1016/j.anaerobe.2016.06.007
Tindall BJ, Rosselló-Móra R, Busse HJ et al (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266. doi:10.1099/ijs.0.016949-0
Turnbaugh PJ, Ley RE, Hamady M et al (2007) The human microbiome project: exploring the microbial part of ourselves in a changing world. Nature 449:804–810. doi:10.1038/nature06244
Turnbaugh PJ, Quince C, Faith JJ et al (2010) Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc Natl Acad Sci USA 107:7503–7508. doi:10.1073/pnas.1002355107
Vandamme P, Coenye T (2004) Taxonomy of the genus cupriavidus: a tale of lost and found. Int J Syst Evol Microbiol 54:2285–2289. doi:10.1099/ijs.0.63247-0
Vandamme P, Peeters C (2014) Time to revisit polyphasic taxonomy. Antonie Van Leeuwenhoek 106:57–65. doi:10.1007/s10482-014-0148x
Vandamme P, Pot B, Gillis M et al (1996) Polyphasic taxonomy, a consensus approach to bacterial systematics. Microbiol Rev 60:407–438
Vanlaere E, Baldwin A, Gevers D et al (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102–111. doi:10.1099/ijs.0.001123-0
Wang Y, Kasper LH (2014) The role of microbiome in central nervous system disorders. Brain Behav Immun 38:1–12. doi:10.1016/j.bbi.2013.12.015
Wayne LG, Brenner DJ, Colwell RR et al (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464
Zhi X-Y, Zhao W, Li W-J, Zhao G-P (2012) Prokaryotic systematics in the genomics era. Antonie Van Leeuwenhoek 101:21–34. doi:10.1007/s10482-011-9667-x
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declares that they do not have conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Abdallah, R.A., Beye, M., Diop, A. et al. The impact of culturomics on taxonomy in clinical microbiology. Antonie van Leeuwenhoek 110, 1327–1337 (2017). https://doi.org/10.1007/s10482-017-0871-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-017-0871-1