Gene-targeted microfluidic cultivation validated by isolation of a gut bacterium listed in human microbiome project's most wanted taxa

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 27, 2014, Pages 9768-9773

  Ma, Liang ^a   Kim, Jungwoo ^a   Hatzenpichler, Roland ^b   Karymov, Mikhail A ^a   Hubert, Nathaniel ^c   Hanan, Ira M ^c   Chang, Eugene B ^c   Ismagilov, Rustem F ^a  

^a California Institute of Technology   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Aerobe; Anaerobe; Cultivate; Metagenome; Microscale

Indexed keywords

BACTERIAL DNA; RNA 16S;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIUM CULTURE; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CECUM; CLOSTRIDIUM; CLOSTRIDIUM SCINDEN; ENTEROCOCCUS FAECALIS; GENE TARGETING; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN TISSUE; INTESTINE BIOPSY; INTESTINE FLORA; MICROFLUIDICS; PRIORITY JOURNAL;

AEROBE; ANAEROBE; CULTIVATE; METAGENOME; MICROSCALE;

GENE TARGETING; HUMANS; INTESTINES; MICROBIOTA; MICROFLUIDIC ANALYTICAL TECHNIQUES; MOLECULAR SEQUENCE DATA;

EID: 84903977458     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1404753111     Document Type: Article

References (43)

1. Schloss PD, Handelsman J (2005) Metagenomics for studying unculturable microorganisms: Cutting the Gordian knot. Genome Biol 6(8):229.
2. Fodor AA, et al. (2012) The "most wanted" taxa from the human microbiome for whole genome sequencing. PLoS ONE 7(7):e41294.
3. Kennedy J, et al. (2011) Functional metagenomic strategies for the discovery of novel enzymes and biosurfactants with biotechnological applications from marine ecosystems. J Appl Microbiol 111(4):787-799.
4. Rooks DJ, McDonald JE, McCarthy AJ (2012) Metagenomic approaches to the discovery of cellulases. Methods Enzymol 510:375-394.
5. Reddy BVB, et al. (2012) Natural product biosynthetic gene diversity in geographically distinct soil microbiomes. Appl Environ Microbiol 78(10):3744-3752.
6. Ridaura VK, et al. (2013) Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341(6150):1241214.
7. Frank DN, et al. (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 104(34):13780-13785. (Pubitemid 350003397)
8. Staley JT, Konopka A (1985) Measurement of in situ activities of nonphotosynthetic microorganisms in aquatic and terrestrial habitats. Annu Rev Microbiol 39(1):321-346.
9. Kaeberlein T, Lewis K, Epstein SS (2002) Isolating " uncultivable" microorganisms in pure culture in a simulated natural environment. Science 296(5570):1127-1129. (Pubitemid 34517131)
10. Stewart EJ (2012) Growing unculturable bacteria. J Bacteriol 194(16):4151-4160.
11. D'Onofrio A, et al. (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17(3):254-264.
12. Giel JL, Sorg JA, Sonenshein AL, Zhu J (2010) Metabolism of bile salts in mice influences spore germination in Clostridium difficile. PLoS ONE 5(1):e8740.
13. Singh S, et al. (2013) Cell extract-containing medium for culture of intracellular fastidious bacteria. J Clin Microbiol 51(8):2599-2607.
14. Zengler K, et al. (2002) Cultivating the uncultured. Proc Natl Acad Sci USA 99(24):15681-15686. (Pubitemid 35403991)
15. Ingham CJ, et al. (2007) The micro-Petri dish, a million-well growth chip for the culture and high-throughput screening of microorganisms. Proc Natl Acad Sci USA 104(46):18217-18222. (Pubitemid 350210847)
16. Eun Y-J, Utada AS, Copeland MF, Takeuchi S, Weibel DB (2011) Encapsulating bacteria in agarose microparticles using microfluidics for high-throughput cell analysis and isolation. ACS Chem Biol 6(3):260-266.
17. Martin K, et al. (2003) Generation of larger numbers of separated microbial populations by cultivation in segmented-flow microdevices. Lab Chip 3(3):202-207. (Pubitemid 41646556)
18. Park J, Kerner A, Burns MA, Lin XN (2011) Microdroplet-enabled highly parallel co-cultivation of microbial communities. PLoS ONE 6(2):e17019.
19. Liu W, Kim HJ, Lucchetta EM, Du W, Ismagilov RF (2009) Isolation, incubation, and parallel functional testing and identification by FISH of rare microbial single-copy cells from multi-species mixtures using the combination of chemistrode and stochastic confinement. Lab Chip 9(15):2153-2162.
20. Vincent ME, Liu W, Haney EB, Ismagilov RF (2010) Microfluidic stochastic confinement enhances analysis of rare cells by isolating cells and creating high density environments for control of diffusible signals. Chem Soc Rev 39(3):974-984.
21. Stevenson BS, Eichorst SA, Wertz JT, Schmidt TM, Breznak JA (2004) New strategies for cultivation and detection of previously uncultured microbes. Appl Environ Microbiol 70(8):4748-4755. (Pubitemid 39095501)
22. Ma L, et al. (2014) Individually addressable arrays of replica microbial cultures enabled by splitting slipchips. Integr Biol, 10.1039/C4IB00109E.
23. Du W, Li L, Nichols KP, Ismagilov RF (2009) SlipChip. Lab Chip 9(16):2286-2292.
24. Shen F, et al. (2010) Nanoliter multiplex PCR arrays on a SlipChip. Anal Chem 82(11):4606-4612.
25. Liu W, Chen D, Du W, Nichols KP, Ismagilov RF (2010) SlipChip for immunoassays in nanoliter volumes. Anal Chem 82(8):3276-3282.
26. Begolo S, Shen F, Ismagilov RF (2013) A microfluidic device for dry sample preservation in remote settings. Lab Chip 13(22):4331-4342.
27. Fuerstman MJ, et al. (2007) The pressure drop along rectangular microchannels containing bubbles. Lab Chip 7(11):1479-1489. (Pubitemid 350013182)
28. Li L, Du W, Ismagilov R (2010) User-loaded SlipChip for equipment-free multiplexed nanoliter-scale experiments. J Am Chem Soc 132(1):106-111.
29. Claesson MJ, et al. (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488(7410):178-184.
30. Raman M, et al. (2013) Fecal microbiome and volatile organic compound metabolome in obese humans with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol 11(7):868-875, e1-e3.
31. Lam YY, et al. (2012) Increased gut permeability and microbiota change associate with mesenteric fat inflammation and metabolic dysfunction in diet-induced obese mice. PLoS ONE 7(3):e34233.
32. Caporaso JG, et al. (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1):4516-4522.
33. Schloss PD, et al. (2009) Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537-7541.
34. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460-2461.
35. Lewis K (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5(1):48-56.
36. Klappenbach JA, Saxman PR, Cole JR, Schmidt TM (2001) Rrndb: The ribosomal RNA operon copy number database. Nucleic Acids Res 29(1):181-184. (Pubitemid 32054441)
37. Amann R, Fuchs BM (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nat Rev Microbiol 6(5):339-348. (Pubitemid 351552655)
38. Stoecker K, Daims H, Wagner M (2005) Fluorescence in situ hybridization for the detection of prokaryotes. Molecular Microbial Ecology, eds Osborn AM, Smith CJ (Bios Advanced Methods, Abingdon, UK), pp 213-239.
39. Amann RI, et al. (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56(6):1919-1925. (Pubitemid 20202165)
40. Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: Development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22(3):434-444. (Pubitemid 29485930)
41. Iino T, Mori K, Tanaka K, Suzuki K, Harayama S (2007) Oscillibacter valericigenes gen. nov., sp. nov., a valerate-producing anaerobic bacterium isolated from the alimentary canal of a Japanese corbicula clam. Int J Syst Evol Microbiol 57(Pt 8):1840-1845. (Pubitemid 47308424)
42. Collins MD, et al. (1994) The phylogeny of the genus Clostridium: Proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44(4):812-826. (Pubitemid 24315163)
43. Yutin N, Galperin MY (2013) A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 15(10):2631-2641.