Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells
Abstract
Here, microbial communities are essential to the function of virtually all ecosystems and eukaryotes, including humans. However, it is still a major challenge to identify microbial cells active under natural conditions in complex systems. Here in this study, we developed a new method to identify and sort active microbes on the single-cell level in complex samples using stable isotope probing with heavy water (D2O) combined with Raman microspectroscopy. Incorporation of D2O-derived D into the biomass of autotrophic and heterotrophic bacteria and archaea could be unambiguously detected via C-D signature peaks in single-cell Raman spectra, and the obtained labeling pattern was confirmed by nanoscale-resolution secondary ion MS. In fast-growing Escherichia coli cells, label detection was already possible after 20 min. For functional analyses of microbial communities, the detection of D incorporation from D2O in individual microbial cells via Raman microspectroscopy can be directly combined with FISH for the identification of active microbes. Applying this approach to mouse cecal microbiota revealed that the host-compound foragers Akkermansia muciniphila and Bacteroides acidifaciens exhibited distinctive response patterns to amendments of mucin and sugars. By Raman-based cell sorting of active (deuterated) cells with optical tweezers and subsequent multiple displacement amplification and DNA sequencing, novel cecal microbesmore »
- Authors:
-
- Division of Microbial Ecology, Department of Microbiology and Ecosystem Science and
- Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China,, Kroto Research Institute and
- Kroto Research Institute and
- Division of Microbial Ecology, Department of Microbiology and Ecosystem Science and, Large Instrument Facility for Advanced Isotope Research, Faculty of Life Sciences, University of Vienna, A-1090 Vienna, Austria,
- Department of Ruminant Sciences, Institute of Animal Science, Agricultural Research Organization, Bet-Dagan 50250, Israel,
- Department of Microbiology, Immunobiology, and Genetics, Max F. Perutz Laboratories, University of Vienna, A-1030 Vienna, Austria,
- Institute of Physical Chemistry and Abbe Center of Photonics, University of Jena, D-07743 Jena, Germany,
- Institute of Physical Chemistry and Abbe Center of Photonics, University of Jena, D-07743 Jena, Germany,, Institute of Photonic Technology, D-07745 Jena, Germany, and
- Department of Chemistry, University of Sheffield, Sheffield S3 7HQ, United Kingdom,
- Kroto Research Institute and, Department of Engineering Science, University of Oxford, Oxford OX1 3PJ, United Kingdom
- Publication Date:
- Research Org.:
- Univ. of Vienna, Vienna (Austria)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1235155
- Alternate Identifier(s):
- OSTI ID: 1342520
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 2; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ecophysiology; single-cell microbiology; carbohydrate utilization; nitrifier; Raman microspectroscopy
Citation Formats
Berry, David, Mader, Esther, Lee, Tae Kwon, Woebken, Dagmar, Wang, Yun, Zhu, Di, Palatinszky, Marton, Schintlmeister, Arno, Schmid, Markus C., Hanson, Buck T., Shterzer, Naama, Mizrahi, Itzhak, Rauch, Isabella, Decker, Thomas, Bocklitz, Thomas, Popp, Jürgen, Gibson, Christopher M., Fowler, Patrick W., Huang, Wei E., and Wagner, Michael. Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells. United States: N. p., 2014.
Web. doi:10.1073/pnas.1420406112.
Berry, David, Mader, Esther, Lee, Tae Kwon, Woebken, Dagmar, Wang, Yun, Zhu, Di, Palatinszky, Marton, Schintlmeister, Arno, Schmid, Markus C., Hanson, Buck T., Shterzer, Naama, Mizrahi, Itzhak, Rauch, Isabella, Decker, Thomas, Bocklitz, Thomas, Popp, Jürgen, Gibson, Christopher M., Fowler, Patrick W., Huang, Wei E., & Wagner, Michael. Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells. United States. https://doi.org/10.1073/pnas.1420406112
Berry, David, Mader, Esther, Lee, Tae Kwon, Woebken, Dagmar, Wang, Yun, Zhu, Di, Palatinszky, Marton, Schintlmeister, Arno, Schmid, Markus C., Hanson, Buck T., Shterzer, Naama, Mizrahi, Itzhak, Rauch, Isabella, Decker, Thomas, Bocklitz, Thomas, Popp, Jürgen, Gibson, Christopher M., Fowler, Patrick W., Huang, Wei E., and Wagner, Michael. Tue .
"Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells". United States. https://doi.org/10.1073/pnas.1420406112.
@article{osti_1235155,
title = {Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells},
author = {Berry, David and Mader, Esther and Lee, Tae Kwon and Woebken, Dagmar and Wang, Yun and Zhu, Di and Palatinszky, Marton and Schintlmeister, Arno and Schmid, Markus C. and Hanson, Buck T. and Shterzer, Naama and Mizrahi, Itzhak and Rauch, Isabella and Decker, Thomas and Bocklitz, Thomas and Popp, Jürgen and Gibson, Christopher M. and Fowler, Patrick W. and Huang, Wei E. and Wagner, Michael},
abstractNote = {Here, microbial communities are essential to the function of virtually all ecosystems and eukaryotes, including humans. However, it is still a major challenge to identify microbial cells active under natural conditions in complex systems. Here in this study, we developed a new method to identify and sort active microbes on the single-cell level in complex samples using stable isotope probing with heavy water (D2O) combined with Raman microspectroscopy. Incorporation of D2O-derived D into the biomass of autotrophic and heterotrophic bacteria and archaea could be unambiguously detected via C-D signature peaks in single-cell Raman spectra, and the obtained labeling pattern was confirmed by nanoscale-resolution secondary ion MS. In fast-growing Escherichia coli cells, label detection was already possible after 20 min. For functional analyses of microbial communities, the detection of D incorporation from D2O in individual microbial cells via Raman microspectroscopy can be directly combined with FISH for the identification of active microbes. Applying this approach to mouse cecal microbiota revealed that the host-compound foragers Akkermansia muciniphila and Bacteroides acidifaciens exhibited distinctive response patterns to amendments of mucin and sugars. By Raman-based cell sorting of active (deuterated) cells with optical tweezers and subsequent multiple displacement amplification and DNA sequencing, novel cecal microbes stimulated by mucin and/or glucosamine were identified, demonstrating the potential of the nondestructive D2O-Raman approach for targeted sorting of microbial cells with defined functional properties for single-cell genomics.},
doi = {10.1073/pnas.1420406112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 2,
volume = 112,
place = {United States},
year = {Tue Dec 30 00:00:00 EST 2014},
month = {Tue Dec 30 00:00:00 EST 2014}
}
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https://doi.org/10.1073/pnas.1420406112
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