Tracking heavy water (D 2 O) incorporation for identifying and sorting active microbial cells

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

doi:10.1073/pnas.1420406112

Title: Tracking heavy water (D ₂ O) incorporation for identifying and sorting active microbial cells

Journal Article · Tue Dec 30 00:00:00 EST 2014 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1420406112· OSTI ID:1235155

Berry, David ^[1]; Mader, Esther ^[1]; Lee, Tae Kwon ^[1]; Woebken, Dagmar ^[1]; Wang, Yun ^[2]; Zhu, Di ^[3]; Palatinszky, Marton ^[1]; Schintlmeister, Arno ^[4]; Schmid, Markus C. ^[1]; Hanson, Buck T. ^[1]; Shterzer, Naama ^[5]; Mizrahi, Itzhak ^[5]; Rauch, Isabella ^[6]; Decker, Thomas ^[6]; Bocklitz, Thomas ^[7]; Popp, Jürgen ^[8]; Gibson, Christopher M. ^[9]; Fowler, Patrick W. ^[9]; Huang, Wei E. ^[10]; Wagner, Michael ^[4]

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

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.

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Research Organization:: Univ. of Vienna, Vienna (Austria)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1235155

Alternate ID(s):: OSTI ID: 1342520

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 112 Journal Issue: 2; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 241 works

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