Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells

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

Volumn 112, Issue 2, 2015, Pages E194-E203

  Berry, David ^a   Mader, Esther ^a   Lee, Tae Kwon ^a   Woebken, Dagmar ^a   Wang, Yun ^b,c   Zhu, Di ^c   Palatinszky, Marton ^a   Schintlmeister, Arno ^a   Schmid, Markus C ^a   Hanson, Buck T ^a   Shterzer, Naama ^d   Mizrahi, Itzhak ^d   Rauch, Isabella ^a   Decker, Thomas ^a   Bocklitz, Thomas ^e   Popp, Jürgen ^e,f   Gibson, Christopher M ^c   Fowler, Patrick W ^c   Huang, Wei E ^c,g   Wagner, Michael ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b QINGDAO INSTITUTE OF BIOENERGY AND BIOPROCESS TECHNOLOGY   (China)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d VOLCANI CENTER   (Israel)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^f LEIBNIZ INSTITUTE OF PHOTONIC TECHNOLOGY   (Germany)

^g UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Carbohydrate utilization; Ecophysiology; Nitrifier; Raman microspectroscopy; Single cell microbiology

Indexed keywords

DEUTERIUM OXIDE; GLUCOSAMINE; MUCIN; ARCHAEAL DNA; BACTERIAL DNA;

ADULT; AKKERMANSIA MUCINIPHILA; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL CELL; BACTEROIDES; BACTEROIDES ACIDIFACIEN; CELL SELECTION; DNA SEQUENCE; ESCHERICHIA COLI; FORAGER; INTESTINE FLORA; MICROBIAL COMMUNITY; MICROBIAL IDENTIFICATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAMAN SPECTROMETRY; ANIMAL; ARCHAEON; BACTERIUM; BIOMASS; C57BL MOUSE; CECUM; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIAL CONSORTIUM; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; MOLECULAR GENETICS; OPTICAL TWEEZERS; PHYLOGENY;

AKKERMANSIA MUCINIPHILA; BACTEROIDES ACIDIFACIENS; ESCHERICHIA COLI; EUKARYOTA;

ANIMALS; ARCHAEA; BACTERIA; BASE SEQUENCE; BIOMASS; CECUM; DEUTERIUM OXIDE; DNA, ARCHAEAL; DNA, BACTERIAL; ESCHERICHIA COLI; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MICE, INBRED C57BL; MICROBIAL CONSORTIA; MICROBIOLOGICAL TECHNIQUES; MOLECULAR SEQUENCE DATA; OPTICAL TWEEZERS; PHYLOGENY; SPECTRUM ANALYSIS, RAMAN;

EID: 84920944435     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1420406112     Document Type: Article

References (110)

1. Frias-Lopez J, et al. (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci USA 105(10):3805-3810.
2. Urich T, et al. (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS ONE 3(6):e2527.
3. VerBerkmoes NC, Denef VJ, Hettich RL, Banfield JF (2009) Systems biology: Functional analysis of natural microbial consortia using community proteomics. Nat Rev Microbiol 7(3):196-205.
4. Adamczyk J, et al. (2003) The isotope array, a new tool that employs substratemediated labeling of rRNA for determination of microbial community structure and function. Appl Environ Microbiol 69(11):6875-6887.
5. Mayali X, et al. (2012) High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use. ISME J 6(6):1210-1221.
6. Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403(6770):646-649.
7. Schwartz E (2007) Characterization of growing microorganisms in soil by stable isotope probing with H2 18O. Appl Environ Microbiol 73(8):2541-2546.
8. Manefield M, Whiteley AS, Griffiths RI, Bailey MJ (2002) RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl Environ Microbiol 68(11):5367-5373.
9. Jehmlich N, Schmidt F, von Bergen M, Richnow HH, Vogt C (2008) Protein-based stable isotope probing (Protein-SIP) reveals active species within anoxic mixed cultures. ISME J 2(11):1122-1133.
10. Pan C, et al. (2011) Quantitative tracking of isotope flows in proteomes of microbial communities. Mol Cell Proteomics 10:M110006049.
11. Almstrand R, Daims H, Persson F, Sörensson F, Hermansson M (2013) New methods for analysis of spatial distribution and coaggregation of microbial populations in complex biofilms. Appl Environ Microbiol 79(19):5978-5987.
12. Skerker JM, Laub MT (2004) Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2(4):325-337.
13. Haider S, et al. (2010) Raman microspectroscopy reveals long-term extracellular activity of Chlamydiae. Mol Microbiol 77(3):687-700.
14. Ackermann M (2013) Microbial individuality in the natural environment. ISME J 7(3): 465-467.
15. Huang WE, et al. (2007) Raman-FISH: Combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ Microbiol 9(8):1878-1889.
16. Wagner M (2009) Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. Annu Rev Microbiol 63:411-429.
17. Dekas AE, Poretsky RS, Orphan VJ (2009) Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326(5951):422-426.
18. Schmid M, Schmitz-Esser S, Jetten M, Wagner M (2001) 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium-oxidizing bacteria: Implications for phylogeny and in situ detection. Environ Microbiol 3(7):450-459.
19. Poulsen LK, Ballard G, Stahl DA (1993) Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms. Appl Environ Microbiol 59(5):1354-1360.
20. Maurice CF, Haiser HJ, Turnbaugh PJ (2013) Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152(1-2):39-50.
21. Blazewicz SJ, Barnard RL, Daly RA, Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: Limitations and uses. ISME J 7(11):2061-2068.
22. Berney M, Hammes F, Bosshard F, Weilenmann H-U, Egli T (2007) Assessment and interpretation of bacterial viability by using the LIVE/DEAD BacLight Kit in combination with flow cytometry. Appl Environ Microbiol 73(10):3283-3290.
23. Hesselsoe M, Nielsen JL, Roslev P, Nielsen PH (2005) Isotope labeling and microautoradiography of active heterotrophic bacteria on the basis of assimilation of 14CO(2). Appl Environ Microbiol 71(2):646-655.
24. 2 assimilation as a measure of metabolic activity in planktonic and sessile bacteria. J Microbiol Methods 59(3):381-393.
25. 2 assimilation by Pseudomonas knackmussii strain B13 and Rhodococcus opacus 1CP and potential impact on biomarker stable isotope probing. Environ Microbiol 10(6):1641-1651.
26. Sorokin JI (1966) On the carbon dioxide uptake during the cell synthesis by microorganisms. Z Allg Mikrobiol 6(1):69-73.
27. Sorokin YI (1966) Role of carbon dioxide and acetate in biosynthesis by sulphatereducing bacteria. Nature 210(5035):551-552.
28. Hatzenpichler R, et al. (2014) In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry. Environ Microbiol 16(8):2568-2590.
29. Kuru E, et al. (2012) In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew Chem Int Ed Engl 51(50):12519-12523.
30. Dumont A, Malleron A, Awwad M, Dukan S, Vauzeilles B (2012) Click-mediated labeling of bacterial membranes through metabolic modification of the lipopolysaccharide inner core. Angew Chem Int Ed Engl 51(13):3143-3146.
31. 2 acetogenesis: Hydrogen utilization efficiency and the origin of lipid-bound hydrogen. Geobiology 2:179-188.
32. Sessions AL, Jahnke LL, Schimmelmann A, Hayes JM (2002) Hydrogen isotope fractionation in lipids of the methane-oxidizing bacterium Methylococcus capsulatus. Geochim Cosmochim Acta 66(22):3955-3969.
33. Zhang X, Gillespie AL, Sessions AL (2009) Large D/H variations in bacterial lipids reflect central metabolic pathways. Proc Natl Acad Sci USA 106(31):12580-12586.
34. Friedman I (1953) Deuterium content of natural waters and other substances. Geochim Cosmochim Acta 4(1-2):89-103.
35. Wegener G, et al. (2012) Assessing sub-seafloor microbial activity by combined stable isotope probing with deuterated water and 13C-bicarbonate. Environ Microbiol 14(6):1517-1527.
36. Kellermann MY, et al. (2012) Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities. Proc Natl Acad Sci USA 109(47):19321-19326.
37. Justice NB, et al. (2014) 15N- and 2H proteomic stable isotope probing links nitrogen flow to archaeal heterotrophic activity. Environ Microbiol 16(10):3224-3237.
38. Brown HC, Bowen RD, Edwards HGM, Farwell DW (2007) Raman spectroscopy of 3-(pent-1-enyl) methyl ether and selected deuterium-labelled analogues. J Raman Spectrosc 38:1586-1594.
39. Bryant GJ, Lavialle F, Levin IW(1982) Effects of membrane bilayer reorganizations on the 2103 cm-1 Raman spectral C-D stretching mode linewidths in dimyristoyl phosphatidylcholine- d54 (DMPC-d54) liposomes. J Raman Spectrosc 12:118-121.
40. Bansil R, Day J, Meadows M, Rice D, Oldfield E (1980) Laser Raman spectroscopic study of specifically deuterated phospholipid bilayers. Biochemistry 19(9):1938-1943.
41. Hill IR, Levin IW (1979) Vibrational spectra and carbon-hydrogen stretching mode assignments for a series of n-alkyl carboxylic acids. J Chem Phys 70(2):842-851.
42. Percot A, Lafleur M (2001) Direct observation of domains in model stratum corneum lipid mixtures by Raman microspectroscopy. Biophys J 81(4):2144-2153.
43. Sagle LB, Zimmermann J, Dawson PE, Romesberg FE (2004) A high-resolution probe of protein folding. J Am Chem Soc 126(11):3384-3385.
44. van Manen H-J, Lenferink A, Otto C (2008) Noninvasive imaging of protein metabolic labeling in single human cells using stable isotopes and Raman microscopy. Anal Chem 80(24):9576-9582.
45. Bremer H, Dennis PP (1996) Escherichia coli and Salmonella: Cellular and Molecular Biology (American Society for Microbiology, Washington, DC), 2nd Ed, pp 1553-1569.
46. Damoglou AP, Dawes EA (1968) Studies on the lipid content and phosphate requirement of glucose-and acetate-grown Escherichia coli. Biochem J 110(4):775-781.
47. Campbell BJ, Li C, Sessions AL, Valentine DL (2009) Hydrogen isotopic fractionation in lipid biosynthesis by H2-consuming Desulfobacterium autotrophicum. Geochim Cosmochim Acta 73:2744-2757.
48. Fischer CR, Bowen BP, Pan C, Northen TR, Banfield JF (2013) Stable-isotope probing reveals that hydrogen isotope fractionation in proteins and lipids in a microbial community are different and species-specific. ACS Chem Biol 8(8):1755-1763.
49. Wales TE, Engen JR (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom Rev 25(1):158-170.
50. Li C, Sessions AL, Kinnaman FS, Valentine DL (2009) Hydrogen-isotopic variability in lipids from Santa Barbara Basin sediments. Geochim Cosmochim Acta 73:4803-4823.
51. Gisolfi CV, Summers RW, Schedl HP, Bleiler TL, Oppliger RA (1990) Human intestinal water absorption: Direct vs. indirect measurements. Am J Physiol 258(2 Pt 1): G216-G222.
52. Thomson JF (1960) Physiological effects of D2O in mammals. Ann N Y Acad Sci 84: 736-744.
53. Lester W Jr, Sun SH, Seber A (1960) Observations on the influence of deuterium on bacterial growth. Ann N Y Acad Sci 84:667-677.
54. Lu MF, Zhang YJ, Zhang HY (2013) Isotope effects on cell growth and sporulation, and spore heat resistance, survival and spontaneous mutation of Bacillus cereus by deuterium oxide culture. Afr J Microbiol Res 7:604-611.
55. Kloss S, et al. (2013) Culture independent Raman spectroscopic identification of urinary tract infection pathogens: A proof of principle study. Anal Chem 85(20): 9610-9616.
56. Kalasinsky KS, et al. (2007) Raman chemical imaging spectroscopy reagentless detection and identification of pathogens: Signature development and evaluation. Anal Chem 79(7):2658-2673.
57. Huang WE, Bailey MJ, Thompson IP, Whiteley AS, Spiers AJ (2007) Single-cell Raman spectral profiles of Pseudomonas fluorescens SBW25 reflects in vitro and in planta metabolic history. Microb Ecol 53(3):414-425.
58. Musat N, Foster R, Vagner T, Adam B, Kuypers MMM (2012) Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol Rev 36(2): 486-511.
59. Woebken D, et al. (2014) Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach. ISME J, 10.1038/ismej.2014.144.
60. Tremaroli V, Bäckhed F (2012) Functional interactions between the gut microbiota and host metabolism. Nature 489(7415):242-249.
61. Weinstock GM (2012) Genomic approaches to studying the human microbiota. Nature 489(7415):250-256.
62. Freter R, Brickner H, Botney M, Cleven D, Aranki A (1983) Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun 39(2):676-685.
63. Stecher B, Berry D, Loy A (2013) Colonization resistance and microbial ecophysiology: Using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle. FEMS Microbiol Rev 37(5):793-829.
64. Ng KM, et al. (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502(7469):96-99.
65. Pacheco AR, et al. (2012) Fucose sensing regulates bacterial intestinal colonization. Nature 492(7427):113-117.
66. Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10(5):323-335.
67. Belzer C, de Vos WM (2012) Microbes inside-From diversity to function: The case of Akkermansia. ISME J 6(8):1449-1458.
68. Berry D, et al. (2013) Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc Natl Acad Sci USA 110(12):4720-4725.
69. Berry D, et al. (2012) Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis. ISME J 6(11):2091-2106.
70. Martens EC, et al. (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9(12):e1001221.
71. Rogers TE, et al. (2013) Dynamic responses of Bacteroides thetaiotaomicron during growth on glycan mixtures. Mol Microbiol 88(5):876-890.
72. Salyers AA, O'Brien M, Kotarski SF (1982) Utilization of chondroitin sulfate by Bacteroides thetaiotaomicron growing in carbohydrate-limited continuous culture. J Bacteriol 150(3):1008-1015.
73. Tsai HH, Hart CA, Rhodes JM (1991) Production of mucin degrading sulphatase and glycosidases by Bacteroides thetaiotaomicron. Lett Appl Microbiol 13(2):97-101.
74. Degnan BA, Macfarlane GT (1995) Carbohydrate utilization patterns and substrate preferences in Bacteroides thetaiotaomicron. Anaerobe 1(1):25-33.
75. Macfarlane GT, Hay S, Macfarlane S, Gibson GR (1990) Effect of different carbohydrates on growth, polysaccharidase and glycosidase production by Bacteroides ovatus, in batch and continuous culture. J Appl Bacteriol 68(2):179-187.
76. Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54(Pt 5):1469-1476.
77. Salyers AA, Vercellotti JR, West SE, Wilkins TD (1977) Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon. Appl Environ Microbiol 33(2):319-322.
78. van Passel MWJ, et al. (2011) The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS ONE 6(3):e16876.
79. Huang WE, Ward AD, Whiteley AS (2009) Raman tweezers sorting of single microbial cells. Environ Microbiol Rep 1(1):44-49.
80. 2O. J Raman Spectrosc 20:683-694.
81. Rinke C, et al. (2014) Obtaining genomes from uncultivated environmental microorganisms using FACS-based single-cell genomics. Nat Protoc 9(5):1038-1048.
82. Park S-K, Kim M-S, Roh SW, Bae J-W (2012) Blautia stercoris sp. nov., isolated from human faeces. Int J Syst Evol Microbiol 62(Pt 4):776-779.
83. Sakamoto M, Benno Y (2006) Reclassification of Bacteroides distasonis, Bacteroides goldsteinii and Bacteroides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae comb. nov. Int J Syst Evol Microbiol 56(Pt 7):1599-1605.
84. Greetham HL, et al. (2004) Allobaculum stercoricanis gen. nov., sp. nov., isolated from canine feces. Anaerobe 10(5):301-307.
85. Sakamoto M, Lan PTN, Benno Y (2007) Barnesiella viscericola gen. nov., sp. nov., a novel member of the family Porphyromonadaceae isolated from chicken caecum. Int J Syst Evol Microbiol 57(Pt 2):342-346.
86. Koskenniemi K, et al. (2011) Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG. Mol Cell Proteomics 10(2): M110002741.
87. Marcy Y, et al. (2007) Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci USA 104(29):11889-11894.
88. Newton DF, Cummings JH, Macfarlane S, Macfarlane GT (1998) Growth of a human intestinal Desulfovibrio desulfuricans in continuous cultures containing defined populations of saccharolytic and amino acid fermenting bacteria. J Appl Microbiol 85(2):372-380.
89. Katz JJ, Crespi HL (1966) Deuterated organisms: Cultivation and uses. Science 151(3715):1187-1194.
90. Katz JJ, Crespi HL, Hasterlik RJ, Thomson JF, Finkel AJ (1957) Some observations on biological effects of deuterium, with special reference to effects on neoplastic processes. J Natl Cancer Inst 18(5):641-659.
91. Matthäus C, et al. (2012) In vivo characterization of atherosclerotic plaque depositions by Raman-probe spectroscopy and in vitro coherent anti-stokes Raman scattering microscopic imaging on a rabbit model. Anal Chem 84(18):7845-7851.
92. Lebedeva EV, et al. (2013) Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon "Ca. Nitrosotenuis uzonensis" representing a clade globally distributed in thermal habitats. PLoS ONE 8(11):e80835.
93. Bassett J, Denney RC, Jeffery GH, Mendham J (1989) Vogel's Textbook of Quantitative Chemical Analysis (Longman, London).
94. Spieck E, et al. (2006) Selective enrichment and molecular characterization of a previously uncultured Nitrospira-like bacterium from activated sludge. Environ Microbiol 8(3):405-415.
95. Leahy SC, et al. (2010) The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS ONE 5(1):e8926.
96. 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.
97. 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.
98. Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM (2008) The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74(5):1646-1648.
99. Stoecker K, Dorninger C, Daims H, Wagner M (2010) Double labeling of oligonucleotide probes for fluorescence in situ hybridization (DOPE-FISH) improves signal intensity and increases rRNA accessibility. Appl Environ Microbiol 76(3):922-926.
100. Bocklitz T, Walter A, Hartmann K, Rösch P, Popp J (2011) How to pre-process Raman spectra for reliable and stable models? Anal Chim Acta 704(1-2):47-56.
101. Ryan CG, Clayton E, Griffin WL, Sie SH, Cousens DR (1988) SNIP, a statistics-sensitive background treatment for the quantitative analysis of PIXE spectra in geoscience applications. Nucl Instrum Methods Phys Res B 34:396-402.
102. Pearson K (1901) On lines and planes of closest fit to systems of points in space. Philos Mag (Abingdon) 2:559-572.
103. Fisher RA (1936) The use of multiple measurements in taxonomic problems. Ann Eugen 7:179-188.
104. Kohavi R (1995) A study of cross-validation and bootstrap for accuracy estimation and model selection. IJCAI (U S) 14:1137-1145.
105. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3): 695-700.
106. Lee SH, Malone C, Kemp PF (1993) Use of multiple 16S rRNA-targeted fluorescent probes to increase signal strength and measure cellular RNA from natural planktonic bacteria. Mar Ecol Prog Ser 101:193-201.
107. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194-2200.
108. Ludwig W, et al. (2004) ARB: A software environment for sequence data. Nucleic Acids Res 32(4):1363-1371.
109. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57(5):758-771.
110. deLaeter JR, et al. (2003) Atomic weights of the elements. Review 2000 (IUPAC Technical Report). Pure Appl Chem 75(6):683-800.