Phenotypic heterogeneity in metabolic traits among single cells of a rare bacterial species in its natural environment quantified with a combination of flow cell sorting and NanoSIMS

Frontiers in Microbiology

Volumn 6, Issue MAR, 2015, Pages

  Zimmermann, M ^a,b   Escrig, S ^c   Hubschmann T ^d   Kirf, M K ^b   Brand, A ^a,b   Inglis, R F ^a,b   Musat, N ^d   Muller S ^d   Meibom, A ^c,e   Ackermann, M ^a,b   Schreiber, F ^a,b  

^a ETH ZURICH   (Switzerland)

^b SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

^c EPFL   (Switzerland)

^d HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Dinitrogen fixation; Diversity; FACS; Green sulfur bacteria; Lago di cadagno; Phenotypic noise; Phenotypic variability; Single cell analysis

Indexed keywords

ARTICLE; BACTERIAL METABOLISM; CARBON DIOXIDE FIXATION; CATALYZED REPORTER DEPOSITION FLUORESCENCE IN SITU HYBRIDIZATION; CELL HETEROGENEITY; CHLOROBIUM; CHLOROBIUM PHAEOBACTEROIDES; CONTROLLED STUDY; CORRELATION ANALYSIS; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; MASS SPECTROMETRY; NANOMETER SCALE SECONDARY ION MASS SPECTROMETRY; NITROGEN FIXATION; NONHUMAN; PHENOTYPE; PHYSICAL CHEMISTRY;

BACTERIA (MICROORGANISMS); CHLOROBI; CHLOROBIUM PHAEOBACTEROIDES;

EID: 84927158514     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00243     Document Type: Article

References (60)

1. Acar, M., Mettetal, J. T., and van Oudenaarden, A. (2008). Stochastic switching as a survival strategy in fluctuating environments. Nat. Genet. 40, 471-475. doi:10.1038/ng.110.
2. Ackermann, M. (2013). Microbial individuality in the natural environment. ISME J. 7, 465-467. doi:10.1038/ismej.2012.131.
3. Ackermann, M., Stecher, B., Freed, N. E., Songhet, P., Hardt, W.-D., and Doebeli, M. (2008). Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987-990. doi:10.1038/nature07067.
4. Arnoldini, M., Vizcarra, I. A., Peña-Miller, R., Stocker, N., Diard, M., Vogel, V., Beardmore, R. E., Hardt, W.-D., and Ackermann, M. (2014). Bistable Expression of Virulence Genes in Salmonella Leads to the Formation of an Antibiotic-Tolerant Subpopulation. PLoS Biol. 12, e1001928. doi:10.1371/journal.pbio.1001928.
5. Balaban, N. Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004). Bacterial Persistence as a Phenotypic Switch. Science (80-. ). 305, 1622-1625. doi:10.1126/science.1099390.
6. Beaumont, H. J. E., Gallie, J., Kost, C., Ferguson, G. C., and Rainey, P. B. (2009). Experimental evolution of bet hedging. Nature 462, 90-93. doi:10.1038/nature08504.
7. Behrens, S., Lösekann, T., Pett-Ridge, J., Weber, P. K., Ng, W.-O., Stevenson, B. S., Hutcheon, I. D., Relman, D. a, and Spormann, A. M. (2008). Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl. Environ. Microbiol. 74, 3143-3150. doi:10.1128/AEM.00191-08.
8. Berry, D., Stecher, B., Schintlmeister, A., Reichert, J., Brugiroux, S., and Wild, B. (2013). Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc. Natl. Acad. Sci. U. S. A., 1-6. doi:10.1073/pnas.1219247110.
9. Biegala, I. C., Not, F., Vaulot, D., and Simon, N. (2003). Quantitative Assessment of Picoeukaryotes in the Natural Environment by Using Taxon-Specific Oligonucleotide Probes in Association with Tyramide Signal Amplification- Fluorescence In Situ Hybridization and Flow Cytometry. Appl. Environ. Microbiol. 69, 5519-5529. doi:10.1128/AEM.69.9.5519.
10. Cline, J. D. (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14, 454-458.
11. Dabundo, R., Lehmann, M. F., Treibergs, L., Tobias, C. R., Altabet, M. A., Moisander, P. H., and Granger, J. (2014). The Contamination of Commercial 15 N 2 Gas Stocks with N - Labeled Nitrate and Ammonium and Consequences for Nitrogen Fixation Measurements. PLoS One 9. doi:10.1371/journal.pone.0110335.
12. Davidson, C. J., and Surette, M. G. (2008). Individuality in Bacteria. Annu. Rev. Genet. 42, 253-268. doi:10.1146/annurev.genet.42.110807.091601.
13. Elowitz, M. B., Levine, A. J., Siggia, E. D., and Swain, P. S. (2002). Stochastic Gene Expression in a Single Cell. Science (80-. ). 297, 1183-1186.
14. Emonet, T., and Cluzel, P. (2008). Relationship between cellular response and behavioral variability in bacterial chemotaxis. Proc. Natl. Acad. Sci. U. S. A. 105, 3304-3309. doi:10.1073/pnas.0705463105.
15. Großkopf, T., Mohr, W., Baustian, T., Schunck, H., Gill, D., Kuypers, M. M. M., Lavik, G., Schmitz, R. A., Wallace, D. W. R., and Laroche, J. (2012). Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488, 361-364. doi:10.1038/nature11338.
16. Halm, H., Musat, N., Lam, P., Langlois, R., Musat, F., Peduzzi, S., Lavik, G., Schubert, C. J., Sinha, B., Singha, B., et al. (2009). Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ. Microbiol. 11, 1945-1958. doi:10.1111/j.1462- 2920.2009.01917.x.
17. Holland, S. L., Reader, T., Dyer, P. S., and Avery, S. V (2014). Phenotypic heterogeneity is a selected trait in natural yeast populations subject to environmental stress. Environ. Microbiol. 16, 1729-1740. doi:10.1111/1462- 2920.12243.
18. Holmes, R. M., Aminot, A., Kerouel, R., Bethanie, H. A., and Peterson, B. J. (1999). A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aquat. Sci. 56, 1801-1808.
19. Hoppe, P., Cohen, S., and Meibom, A. (2013). NanoSIMS: Technical Aspects and Applications in Cosmochemistry and Biological Geochemistry. Geostand. Geoanalytical Res. 37, 111-154. doi:10.1111/j.1751-908X.2013.00239.x.
20. Kashtan, N., Roggensack, S. E., Rodrigue, S., Thompson, J. W., Biller, S. J., Coe, A., Ding, H., Marttinen, P., Malmstrom, R. R., Stocker, R., et al. (2014). Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus. Science (80-. ). 344, 416-419. doi:10.1126/science.1248575.
21. Kirf, M. K., Dinkel, C., Schubert, C. J., and Wehrli, B. (2013). Submicromolar Oxygen Profiles at the Oxic-Anoxic Boundary of Temperate Lakes. Aquat. Geochemistry 20, 39-57. doi:10.1007/s10498-013-9206-7.
22. Kiviet, D. J., Nghe, P., Walker, N., Boulineau, S., Sunderlikova, V., and Tans, S. J. (2014). Stochasticity of metabolism and growth at the single-cell level. Nature, doi:10.1038/nature13582. doi:10.1038/nature13582.
23. Koch, C., Günther, S., Desta, A. F., Hübschmann, T., and Müller, S. (2013). Cytometric fingerprinting for analyzing microbial intracommunity structure variation and identifying subcommunity function. Nat. Protoc. 8, 190-202. doi:10.1038/nprot.2012.149.
24. Korobkova, E., Emonet, T., Vilar, J. M. G., Shimizu, T. S., and Cluzel, P. (2004). From molecular noise to behavioural variability in a single bacterium. Nature 428, 574-577. doi:10.1074/jbc.C300557200.
25. Kotte, O., Volkmer, B., Radzikowski, J. L., and Heinemann, M. (2014). Phenotypic bistability in Escherichia coli ' s central carbon metabolism. Mol. Syst. Biol. 10, 1-11.
26. Kussell, E., and Leibler, S. (2005). Phenotypic Diversity , Population Growth , and Information in Fluctuating Environments. Science (80-. ). 309, 2075-2078. doi:10.1126/science.1114383.
27. Lechene, C., Hillion, F., Mcmahon, G., Benson, D., Kleinfeld, A. M., Kampf, J. P., Distel, D., Luyten, Y., Bonventre, J., Hentschel, D., et al. (2006). Highresolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J. Biol. 5, 1-30.
28. Lechene, C. P., Luyten, Y., McMahon, G., and Distel, D. L. (2007). Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science (80-. ). 317, 1563-1566. doi:10.1126/science.1145557.
29. Levy, S. F., Ziv, N., and Siegal, M. L. (2012). Bet hedging in yeast by heterogeneous, age-correlated expression of a stress protectant. PLoS Biol. 10, e1001325. doi:10.1371/journal.pbio.1001325.
30. Lomas, M. W., Bronk, D. a, and van den Engh, G. (2011). Use of flow cytometry to measure biogeochemical rates and processes in the ocean. Ann. Rev. Mar. Sci. 3, 537-566. doi:10.1146/annurev-marine-120709-142834.
31. Maamar, H., Raj, A., and Dubnau, D. (2007). Noise in gene expression determines cell fate in Bacillus subtilis. Science (80-. ). 317, 526-529. doi:10.1126/science.1140818.
32. Mohr, W., Grosskopf, T., Wallace, D. W. R., and LaRoche, J. (2010). Methodological underestimation of oceanic nitrogen fixation rates. PLoS One 5, e12583. doi:10.1371/journal.pone.0012583.
33. Mou, X., Hodson, R. E., and Moran, M. A. (2007). Bacterioplankton assemblages transforming dissolved organic compounds in coastal seawater. Environ. Microbiol. 9, 2025-2037. doi:10.1111/j.1462-2920.2007.01318.x.
34. Müller, S., and Nebe-von-Caron, G. (2010). Functional single-cell analyses: flow cytometry and cell sorting of microbial populations and communities. FEMS Microbiol. Rev. 34, 554-587. doi:10.1111/j.1574-6976.2010.00214.x.
35. Musat, N., Foster, R., Vagner, T., Adam, B., and Kuypers, M. M. M. (2012). Detecting metabolic activities in single cells, with emphasis on nanoSIMS. FEMS Microbiol. Rev. 36, 486-511. doi:10.1111/j.1574-6976.2011.00303.x.
36. Musat, N., Halm, H., Winterholler, B., Hoppe, P., Peduzzi, S., Hillion, F., Horreard, F., Amann, R., Jørgensen, B. B., and Kuypers, M. M. M. (2008). A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc. Natl. Acad. Sci. U. S. A. 105, 17861-17866. doi:10.1073/pnas.0809329105.
37. New, A. M., Cerulus, B., Govers, S. K., Perez-Samper, G., Zhu, B., Boogmans, S., Xavier, J. B., and Verstrepen, K. J. (2014). Different levels of catabolite repression optimize growth in stable and variable environments. PLoS Biol. 12, e1001764. doi:10.1371/journal.pbio.1001764.
38. Nordlund, S., and Högbom, M. (2013). ADP-ribosylation, a mechanism regulating nitrogenase activity. FEBS J. 280, 3484-3490. doi:10.1111/febs.12279.
39. Ozbudak, E. M., Thattai, M., Kurtser, I., Grossman, A. D., and Oudenaarden, A. Van (2002). Regulation of noise in the expression of a single gene. Nat. Genet. 31, 69-73. doi:10.1038/ng869.
40. Ozbudak, E. M., Thattai, M., Lim, H. N., Shraiman, B. I., and Van Oudenaarden, A. (2004). Multistability in the lactose utilization network of Escherichia coli. Nature 427, 737-40. doi:10.1038/nature02298.
41. Pedros-Alio, C. (2012). The Rare Bacterial Biosphere. Ann. Rev. Mar. Sci. 4, 449- 466. doi:10.1146/annurev-marine-120710-100948.
42. Polerecky, L., Adam, B., Milucka, J., Musat, N., Vagner, T., and Kuypers, M. M. M. (2012). Look@NanoSIMS-a tool for the analysis of nanoSIMS data in environmental microbiology. Environ. Microbiol. 14, 1009-1023. doi:10.1111/j.1462-2920.2011.02681.x.
43. Raj, A., and van Oudenaarden, A. (2008). Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135, 216-26. doi:10.1016/j.cell.2008.09.050.
44. Ratcliff, W. C., and Denison, R. F. (2010). Individual-level bet hedging in the bacterium Sinorhizobium meliloti. Curr. Biol. 20, 1740-1744. doi:10.1016/j.cub.2010.08.036.
45. Sekar, R., Fuchs, B. M., Amann, R., and Pernthaler, J. (2004). Flow Sorting of Marine Bacterioplankton after Fluorescence In Situ Hybridization. Appl. Environ. Microbiol. 70, 6210-6219. doi:10.1128/AEM.70.10.6210.
46. Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse, S. M., Neal, P. R., Arrieta, J. M., and Herndl, G. J. (2006). Microbial diversity in the deep sea and the underexplored "' rare biosphere .'" Proc. Natl. Acad. Sci. U. S. A. 103, 12115-12120.
47. Solopova, A., van Gestel, J., Weissing, F. J., Bachmann, H., Teusink, B., Kok, J., and Kuipers, O. P. (2014). Bet-hedging during bacterial diauxic shift. Proc. Natl. Acad. Sci. U. S. A. 111, 7427-7432. doi:10.1073/pnas.1320063111.
48. Tada, Y., and Grossart, H.-P. (2014). Community shifts of actively growing lake bacteria after N-acetyl-glucosamine addition: improving the BrdU-FACS method. ISME J. 8, 441-454. doi:10.1038/ismej.2013.148.
49. Thompson, A. W., Foster, R. A., Krupke, A., Carter, B. J., Musat, N., Vaulot, D., Kuypers, M. M. M., and Zehr, J. P. (2012). Unicellular Cyanobacterium Symbiotic with a Single-Celled Eukaryotic Alga. Science (80-. ). 377, 1546- 1549. doi:10.1126/science.1222700.
50. Thompson, J. R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D. E., Benoit, J., Sarma-Rupavtarm, R., Distel, D. L., and Polz, M. F. (2005). Genotypic Diversity Within a Natural Coastal Bacterioplankton Population. Science (80-. ). 307, 1311-1313. doi:10.1126/science.1106028.
51. Tonolla, M., Peduzzi, S., Hahn, D., and Peduzzi, R. (2003). Spatio-temporal distribution of phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno (Switzerland). FEMS Microbiol. Ecol. 43, 89-98. doi:10.1111/j.1574- 6941.2003.tb01048.x.
52. Veening, J.-W., Stewart, E. J., Berngruber, T. W., Taddei, F., Kuipers, O. P., and Hamoen, L. W. (2008). Bet-hedging and epigenetic inheritance in bacterial cell development. Proc. Natl. Acad. Sci. U. S. A. 105, 4393-4398. doi:10.1073/pnas.0700463105.
53. Wakamoto, Y., Dhar, N., Chait, R., Schneider, K., Signorino-Gelo, F., Leibler, S., and McKinney, J. D. (2013). Dynamic persistence of antibiotic-stressed mycobacteria. Science (80-. ). 339, 91-95. doi:10.1126/science.1229858.
54. Woebken, D., Burow, L. C., Behnam, F., Mayali, X., Schintlmeister, A., Fleming, E. D., Prufert-bebout, L., Singer, S. W., Hoehler, T. M., Pett-ridge, J., et al. (2014). Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach. ISME J., doi: 10.1038/ismej.2014.144. doi:10.1038/ismej.2014.144.
55. Woebken, D., Burow, L. C., Prufert-Bebout, L., Bebout, B. M., Hoehler, T. M., Pett- Ridge, J., Spormann, A. M., Weber, P. K., and Singer, S. W. (2012). Identification of a novel cyanobacterial group as active diazotrophs in a coastal microbial mat using NanoSIMS analysis. ISME J. 6, 1427-1439. doi:10.1038/ismej.2011.200.
56. Yilmaz, S., Haroon, M. F., Rabkin, B. A., Tyson, G. W., and Hugenholtz, P. (2010). Fixation-free fluorescence in situ hybridization for targeted enrichment of microbial populations. ISME J 4, 1352-1356. doi:10.1038/ismej.2010.73.
57. Young, J. W., Locke, J. C. W., Altinok, A., Rosenfeld, N., Bacarian, T., Swain, P. S., Mjolsness, E., and Elowitz, M. B. (2012). Measuring single-cell gene expression dynamics in bacteria using fluorescence time-lapse microscopy. Nat. Protoc. 7, 80-88. doi:10.1038/nprot.2011.432.
58. Ziv, N., Siegal, M. L., and Gresham, D. (2013). Genetic and nongenetic determinants of cell growth variation assessed by high-throughput microscopy. Mol. Biol. Evol. 30, 2568-2578. doi:10.1093/molbev/mst138.
59. Zubkov, M. V, Fuchs, B. M., Tarran, G. A., Burkill, P. H., and Amann, R. (2003). High Rate of Uptake of Organic Nitrogen Compounds by Prochlorococcus Cyanobacteria as a Key to Their Dominance in Oligotrophic Oceanic Waters. Appl. Environ. Microbiol. 69, 1299-1304. doi:10.1128/AEM.69.2.1299.
60. Zubkov, M. V., Fuchs, B. M., Burkill, P. H., and Amann, R. (2001). Comparison of Cellular and Biomass Specific Activities of Dominant Bacterioplankton Groups in Stratified Waters of the Celtic Sea. Appl. Environ. Microbiol. 67, 5210-5218. doi:10.1128/AEM.67.11.5210-5218.2001.