Abstract

Denitrifying anaerobic methane oxidizing (DAMO) microorganisms play an important role in the global carbon and nitrogen cycles as they are able to mediate methane oxidation using nitrite/nitrate under anoxic conditions. However, the physiological properties of DAMO microorganisms remain poorly understood, partially since the organisms are difficult to isolate or cultivate in pure culture and partially because of their long cultivation time. In this study, DAMO cell sorting has been conducted by integrating optical tweezers within enclosed microfluidic chips. This integrated cell sorting method has high purity, low infection rates, and causes no discernable harm to cell viability. The purity of the sorted cells was controlled by the microfluidic chip structure design and operation, while the cell viability was verified by imaging the cultured DAMO archaea after 420 days.

© 2017 Optical Society of America

Full Article  |  PDF Article

Corrections

6 February 2017: A correction was made to the author listing.


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References

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2014 (4)

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
[Crossref] [PubMed]

X. Qi, T. A. Nieminen, A. B. Stilgoe, V. L. Loke, and H. Rubinsztein-Dunlop, “Comparison of T-matrix calculation methods for scattering by cylinders in optical tweezers,” Opt. Lett. 39(16), 4827–4830 (2014).
[Crossref] [PubMed]

X. Chen, J. Guo, Y. Shi, S. Hu, Z. Yuan, and B.-J. Ni, “Modeling of simultaneous anaerobic methane and ammonium oxidation in a membrane biofilm reactor,” Environ. Sci. Technol. 48(16), 9540–9547 (2014).
[Crossref] [PubMed]

J. S. Deutzmann, P. Stief, J. Brandes, and B. Schink, “Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake,” Proc. Natl. Acad. Sci. U.S.A. 111(51), 18273–18278 (2014).
[Crossref] [PubMed]

2013 (5)

C. Muhiddin, D. B. Phillips, M. J. Miles, L. Picco, and D. M. Carberry, “Kinect 4 ... holographic optical tweezers,” J. Opt. 15(7), 075302 (2013).
[Crossref]

C. McDonald, M. McPherson, C. McDougall, and D. McGloin, “Holohands: games console interface for controlling holographic optical manipulation,” J. Opt. 15(3), 035708 (2013).
[Crossref]

M. F. Haroon, S. Hu, Y. Shi, M. Imelfort, J. Keller, P. Hugenholtz, Z. Yuan, and G. W. Tyson, “Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage,” Nature 500(7464), 567–570 (2013).
[Crossref] [PubMed]

T. Nawy, “Single-cell sequencing,” Nat. Methods 11(1), 18 (2013).
[Crossref] [PubMed]

Z. C. Landry, S. J. Giovanonni, S. R. Quake, and P. C. Blainey, “Optofluidic cell selection from complex microbial communities for single-genome analysis,” Methods Enzymol. 531, 61–90 (2013).

2011 (2)

X. Wang, S. Chen, M. Kong, Z. Wang, K. D. Costa, R. A. Li, and D. Sun, “Enhanced cell sorting and manipulation with combined optical tweezer and microfluidic chip technologies,” Lab Chip 11(21), 3656–3662 (2011).
[Crossref] [PubMed]

S. Hu, R. J. Zeng, J. Keller, P. A. Lant, and Z. Yuan, “Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process,” Environ. Microbiol. Rep. 3(3), 315–319 (2011).
[Crossref] [PubMed]

2010 (1)

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
[Crossref] [PubMed]

2009 (6)

K. Knittel and A. Boetius, “Anaerobic oxidation of methane: progress with an unknown process,” Annu. Rev. Microbiol. 63(1), 311–334 (2009).
[Crossref] [PubMed]

K. Gassei, J. Ehmcke, and S. Schlatt, “Efficient enrichment of undifferentiated GFR alpha 1(+) spermatogonia from immature rat testis by magnetic activated cell sorting,” Cell Tissue Res. 337(1), 177–183 (2009).
[Crossref] [PubMed]

C. Y. Fong, G. S. L. Peh, K. Gauthaman, and A. Bongso, “Separation of SSEA-4 and TRA-1-60 labelled undifferentiated human embryonic stem cells from a heterogeneous cell population using magnetic-activated cell sorting (MACS) and fluorescence-activated cell sorting (FACS),” Stem Cell Rev. 5(1), 72–80 (2009).
[Crossref] [PubMed]

I. Perch-Nielsen, D. Palima, J. S. Dam, and J. Glückstad, “Parallel particle identification and separation for active optical sorting,” J. Opt. A, Pure Appl. Opt. 11(3), 034013 (2009).
[Crossref]

J. A. Grieve, A. Ulcinas, S. Subramanian, G. M. Gibson, M. J. Padgett, D. M. Carberry, and M. J. Miles, “Hands-on with optical tweezers: a multitouch interface for holographic optical trapping,” Opt. Express 17(5), 3595–3602 (2009).
[Crossref] [PubMed]

K. F. Ettwig, T. van Alen, K. T. van de Pas-Schoonen, M. S. Jetten, and M. Strous, “Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum,” Appl. Environ. Microbiol. 75(11), 3656–3662 (2009).
[Crossref] [PubMed]

2008 (1)

T. D. Perroud, J. N. Kaiser, J. C. Sy, T. W. Lane, C. S. Branda, A. K. Singh, and K. D. Patel, “Microfluidic-based cell sorting of Francisella tularensis infected macrophages using optical forces,” Anal. Chem. 80(16), 6365–6372 (2008).
[Crossref] [PubMed]

2007 (2)

S. Higuchi, T. Hayashi, I. Hori, N. Shibata, H. Sakamoto, and K. Agata, “Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis,” Dev. Growth Differ. 49(7), 571–581 (2007).
[Crossref] [PubMed]

T. A. Nieminen, V. L. Loke, A. B. Stilgoe, G. Knöner, A. M. Brańczyk, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical tweezers computational toolbox,” J. Opt. A, Pure Appl. Opt. 9(8), S196–S203 (2007).
[Crossref]

2006 (1)

A. A. Raghoebarsing, A. Pol, K. T. van de Pas-Schoonen, A. J. P. Smolders, K. F. Ettwig, W. I. C. Rijpstra, S. Schouten, J. S. S. Damsté, H. J. M. Op den Camp, M. S. M. Jetten, and M. Strous, “A microbial consortium couples anaerobic methane oxidation to denitrification,” Nature 440(7086), 918–921 (2006).
[Crossref] [PubMed]

2005 (2)

J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
[Crossref] [PubMed]

C. Xie, D. Chen, and Y. Q. Li, “Raman sorting and identification of single living micro-organisms with optical tweezers,” Opt. Lett. 30(14), 1800–1802 (2005).
[Crossref] [PubMed]

2003 (3)

M. P. MacDonald, G. C. Spalding, and K. Dholakia, “Microfluidic sorting in an optical lattice,” Nature 426(6965), 421–424 (2003).
[Crossref] [PubMed]

S. K. Sia and G. M. Whitesides, “Microfluidic devices fabricated in poly(dimethylsiloxane) for biological studies,” Electrophoresis 24(21), 3563–3576 (2003).
[Crossref] [PubMed]

S. K. Cho, H. J. Moon, and C. J. Kim, “Creating, transporting, cutting, and merging liquid droplets by electrowetting- based actuation for digital microfluidic circuits,” J. Microelectromech. Syst. 12(1), 70–80 (2003).
[Crossref]

2001 (1)

J. C. Love, J. R. Anderson, and G. M. Whitesides, “Fabrication of three-dimensional microfluidic systems by soft lithography,” MRS Bull. 26(07), 523–528 (2001).
[Crossref]

1995 (1)

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-IR microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

1994 (1)

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct. 23(1), 247–285 (1994).
[Crossref] [PubMed]

1990 (1)

R. I. Amann, L. Krumholz, and D. A. Stahl, “Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology,” J. Bacteriol. 172(2), 762–770 (1990).
[Crossref] [PubMed]

1986 (1)

Agata, K.

S. Higuchi, T. Hayashi, I. Hori, N. Shibata, H. Sakamoto, and K. Agata, “Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis,” Dev. Growth Differ. 49(7), 571–581 (2007).
[Crossref] [PubMed]

Amann, R. I.

R. I. Amann, L. Krumholz, and D. A. Stahl, “Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology,” J. Bacteriol. 172(2), 762–770 (1990).
[Crossref] [PubMed]

Ananthakrishnan, R.

J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
[Crossref] [PubMed]

Anderson, J. R.

J. C. Love, J. R. Anderson, and G. M. Whitesides, “Fabrication of three-dimensional microfluidic systems by soft lithography,” MRS Bull. 26(07), 523–528 (2001).
[Crossref]

Ashkin, A.

Bernard, V.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
[Crossref] [PubMed]

Berns, M. W.

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-IR microbeams,” Nature 377(6544), 20–21 (1995).
[Crossref] [PubMed]

Biesemann, C.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
[Crossref] [PubMed]

Bilby, C.

J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
[Crossref] [PubMed]

Bjorkholm, J. E.

Blainey, P. C.

Z. C. Landry, S. J. Giovanonni, S. R. Quake, and P. C. Blainey, “Optofluidic cell selection from complex microbial communities for single-genome analysis,” Methods Enzymol. 531, 61–90 (2013).

Block, S. M.

K. Svoboda and S. M. Block, “Biological applications of optical forces,” Annu. Rev. Biophys. Biomol. Struct. 23(1), 247–285 (1994).
[Crossref] [PubMed]

Boetius, A.

K. Knittel and A. Boetius, “Anaerobic oxidation of methane: progress with an unknown process,” Annu. Rev. Microbiol. 63(1), 311–334 (2009).
[Crossref] [PubMed]

Bongso, A.

C. Y. Fong, G. S. L. Peh, K. Gauthaman, and A. Bongso, “Separation of SSEA-4 and TRA-1-60 labelled undifferentiated human embryonic stem cells from a heterogeneous cell population using magnetic-activated cell sorting (MACS) and fluorescence-activated cell sorting (FACS),” Stem Cell Rev. 5(1), 72–80 (2009).
[Crossref] [PubMed]

Branczyk, A. M.

T. A. Nieminen, V. L. Loke, A. B. Stilgoe, G. Knöner, A. M. Brańczyk, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical tweezers computational toolbox,” J. Opt. A, Pure Appl. Opt. 9(8), S196–S203 (2007).
[Crossref]

Branda, C. S.

T. D. Perroud, J. N. Kaiser, J. C. Sy, T. W. Lane, C. S. Branda, A. K. Singh, and K. D. Patel, “Microfluidic-based cell sorting of Francisella tularensis infected macrophages using optical forces,” Anal. Chem. 80(16), 6365–6372 (2008).
[Crossref] [PubMed]

Brandes, J.

J. S. Deutzmann, P. Stief, J. Brandes, and B. Schink, “Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake,” Proc. Natl. Acad. Sci. U.S.A. 111(51), 18273–18278 (2014).
[Crossref] [PubMed]

Brose, N.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
[Crossref] [PubMed]

Bungers, S. R.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
[Crossref] [PubMed]

Butler, M. K.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
[Crossref] [PubMed]

Byrne, J. A.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
[Crossref] [PubMed]

Carberry, D. M.

Chen, D.

Chen, S.

X. Wang, S. Chen, M. Kong, Z. Wang, K. D. Costa, R. A. Li, and D. Sun, “Enhanced cell sorting and manipulation with combined optical tweezer and microfluidic chip technologies,” Lab Chip 11(21), 3656–3662 (2011).
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X. Chen, J. Guo, Y. Shi, S. Hu, Z. Yuan, and B.-J. Ni, “Modeling of simultaneous anaerobic methane and ammonium oxidation in a membrane biofilm reactor,” Environ. Sci. Technol. 48(16), 9540–9547 (2014).
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S. K. Cho, H. J. Moon, and C. J. Kim, “Creating, transporting, cutting, and merging liquid droplets by electrowetting- based actuation for digital microfluidic circuits,” J. Microelectromech. Syst. 12(1), 70–80 (2003).
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Chu, S.

Cooper, B.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
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X. Wang, S. Chen, M. Kong, Z. Wang, K. D. Costa, R. A. Li, and D. Sun, “Enhanced cell sorting and manipulation with combined optical tweezer and microfluidic chip technologies,” Lab Chip 11(21), 3656–3662 (2011).
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I. Perch-Nielsen, D. Palima, J. S. Dam, and J. Glückstad, “Parallel particle identification and separation for active optical sorting,” J. Opt. A, Pure Appl. Opt. 11(3), 034013 (2009).
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de Beer, D.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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J. S. Deutzmann, P. Stief, J. Brandes, and B. Schink, “Anaerobic methane oxidation coupled to denitrification is the dominant methane sink in a deep lake,” Proc. Natl. Acad. Sci. U.S.A. 111(51), 18273–18278 (2014).
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M. P. MacDonald, G. C. Spalding, and K. Dholakia, “Microfluidic sorting in an optical lattice,” Nature 426(6965), 421–424 (2003).
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Dutilh, B. E.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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Ebert, S.

J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
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K. Gassei, J. Ehmcke, and S. Schlatt, “Efficient enrichment of undifferentiated GFR alpha 1(+) spermatogonia from immature rat testis by magnetic activated cell sorting,” Cell Tissue Res. 337(1), 177–183 (2009).
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J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
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K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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K. Gassei, J. Ehmcke, and S. Schlatt, “Efficient enrichment of undifferentiated GFR alpha 1(+) spermatogonia from immature rat testis by magnetic activated cell sorting,” Cell Tissue Res. 337(1), 177–183 (2009).
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C. Y. Fong, G. S. L. Peh, K. Gauthaman, and A. Bongso, “Separation of SSEA-4 and TRA-1-60 labelled undifferentiated human embryonic stem cells from a heterogeneous cell population using magnetic-activated cell sorting (MACS) and fluorescence-activated cell sorting (FACS),” Stem Cell Rev. 5(1), 72–80 (2009).
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Giovanonni, S. J.

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K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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I. Perch-Nielsen, D. Palima, J. S. Dam, and J. Glückstad, “Parallel particle identification and separation for active optical sorting,” J. Opt. A, Pure Appl. Opt. 11(3), 034013 (2009).
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Grønborg, M.

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X. Chen, J. Guo, Y. Shi, S. Hu, Z. Yuan, and B.-J. Ni, “Modeling of simultaneous anaerobic methane and ammonium oxidation in a membrane biofilm reactor,” Environ. Sci. Technol. 48(16), 9540–9547 (2014).
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M. F. Haroon, S. Hu, Y. Shi, M. Imelfort, J. Keller, P. Hugenholtz, Z. Yuan, and G. W. Tyson, “Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage,” Nature 500(7464), 567–570 (2013).
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C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
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Hu, S.

X. Chen, J. Guo, Y. Shi, S. Hu, Z. Yuan, and B.-J. Ni, “Modeling of simultaneous anaerobic methane and ammonium oxidation in a membrane biofilm reactor,” Environ. Sci. Technol. 48(16), 9540–9547 (2014).
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M. F. Haroon, S. Hu, Y. Shi, M. Imelfort, J. Keller, P. Hugenholtz, Z. Yuan, and G. W. Tyson, “Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage,” Nature 500(7464), 567–570 (2013).
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S. Hu, R. J. Zeng, J. Keller, P. A. Lant, and Z. Yuan, “Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process,” Environ. Microbiol. Rep. 3(3), 315–319 (2011).
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Hugenholtz, P.

M. F. Haroon, S. Hu, Y. Shi, M. Imelfort, J. Keller, P. Hugenholtz, Z. Yuan, and G. W. Tyson, “Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage,” Nature 500(7464), 567–570 (2013).
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Imelfort, M.

M. F. Haroon, S. Hu, Y. Shi, M. Imelfort, J. Keller, P. Hugenholtz, Z. Yuan, and G. W. Tyson, “Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage,” Nature 500(7464), 567–570 (2013).
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Jahn, O.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
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Janssen-Megens, E. M.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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Jetten, M. S.

K. F. Ettwig, T. van Alen, K. T. van de Pas-Schoonen, M. S. Jetten, and M. Strous, “Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum,” Appl. Environ. Microbiol. 75(11), 3656–3662 (2009).
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Jetten, M. S. M.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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A. A. Raghoebarsing, A. Pol, K. T. van de Pas-Schoonen, A. J. P. Smolders, K. F. Ettwig, W. I. C. Rijpstra, S. Schouten, J. S. S. Damsté, H. J. M. Op den Camp, M. S. M. Jetten, and M. Strous, “A microbial consortium couples anaerobic methane oxidation to denitrification,” Nature 440(7086), 918–921 (2006).
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T. D. Perroud, J. N. Kaiser, J. C. Sy, T. W. Lane, C. S. Branda, A. K. Singh, and K. D. Patel, “Microfluidic-based cell sorting of Francisella tularensis infected macrophages using optical forces,” Anal. Chem. 80(16), 6365–6372 (2008).
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Käs, J.

J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
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Keller, J.

M. F. Haroon, S. Hu, Y. Shi, M. Imelfort, J. Keller, P. Hugenholtz, Z. Yuan, and G. W. Tyson, “Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage,” Nature 500(7464), 567–570 (2013).
[Crossref] [PubMed]

S. Hu, R. J. Zeng, J. Keller, P. A. Lant, and Z. Yuan, “Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process,” Environ. Microbiol. Rep. 3(3), 315–319 (2011).
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Kim, C. J.

S. K. Cho, H. J. Moon, and C. J. Kim, “Creating, transporting, cutting, and merging liquid droplets by electrowetting- based actuation for digital microfluidic circuits,” J. Microelectromech. Syst. 12(1), 70–80 (2003).
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K. Knittel and A. Boetius, “Anaerobic oxidation of methane: progress with an unknown process,” Annu. Rev. Microbiol. 63(1), 311–334 (2009).
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T. A. Nieminen, V. L. Loke, A. B. Stilgoe, G. Knöner, A. M. Brańczyk, N. R. Heckenberg, and H. Rubinsztein-Dunlop, “Optical tweezers computational toolbox,” J. Opt. A, Pure Appl. Opt. 9(8), S196–S203 (2007).
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Kong, M.

X. Wang, S. Chen, M. Kong, Z. Wang, K. D. Costa, R. A. Li, and D. Sun, “Enhanced cell sorting and manipulation with combined optical tweezer and microfluidic chip technologies,” Lab Chip 11(21), 3656–3662 (2011).
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König, K.

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-IR microbeams,” Nature 377(6544), 20–21 (1995).
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Krumholz, L.

R. I. Amann, L. Krumholz, and D. A. Stahl, “Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology,” J. Bacteriol. 172(2), 762–770 (1990).
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Kuypers, M. M. M.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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Landry, Z. C.

Z. C. Landry, S. J. Giovanonni, S. R. Quake, and P. C. Blainey, “Optofluidic cell selection from complex microbial communities for single-genome analysis,” Methods Enzymol. 531, 61–90 (2013).

Lane, T. W.

T. D. Perroud, J. N. Kaiser, J. C. Sy, T. W. Lane, C. S. Branda, A. K. Singh, and K. D. Patel, “Microfluidic-based cell sorting of Francisella tularensis infected macrophages using optical forces,” Anal. Chem. 80(16), 6365–6372 (2008).
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Lant, P. A.

S. Hu, R. J. Zeng, J. Keller, P. A. Lant, and Z. Yuan, “Effect of nitrate and nitrite on the selection of microorganisms in the denitrifying anaerobic methane oxidation process,” Environ. Microbiol. Rep. 3(3), 315–319 (2011).
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Le Paslier, D.

K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
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C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
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Li, R. A.

X. Wang, S. Chen, M. Kong, Z. Wang, K. D. Costa, R. A. Li, and D. Sun, “Enhanced cell sorting and manipulation with combined optical tweezer and microfluidic chip technologies,” Lab Chip 11(21), 3656–3662 (2011).
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Liang, H.

K. König, H. Liang, M. W. Berns, and B. J. Tromberg, “Cell damage by near-IR microbeams,” Nature 377(6544), 20–21 (1995).
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J. Guck, S. Schinkinger, B. Lincoln, F. Wottawah, S. Ebert, M. Romeyke, D. Lenz, H. M. Erickson, R. Ananthakrishnan, D. Mitchell, J. Käs, S. Ulvick, and C. Bilby, “Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence,” Biophys. J. 88(5), 3689–3698 (2005).
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K. F. Ettwig, M. K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M. M. M. Kuypers, F. Schreiber, B. E. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, H. J. Wessels, T. van Alen, F. Luesken, M. L. Wu, K. T. van de Pas-Schoonen, H. J. Op den Camp, E. M. Janssen-Megens, K. J. Francoijs, H. Stunnenberg, J. Weissenbach, M. S. M. Jetten, and M. Strous, “Nitrite-driven anaerobic methane oxidation by oxygenic bacteria,” Nature 464(7288), 543–548 (2010).
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Luquet, E.

C. Biesemann, M. Grønborg, E. Luquet, S. P. Wichert, V. Bernard, S. R. Bungers, B. Cooper, F. Varoqueaux, L. Li, J. A. Byrne, H. Urlaub, O. Jahn, N. Brose, and E. Herzog, “Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting,” EMBO J. 33(2), 157–170 (2014).
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M. P. MacDonald, G. C. Spalding, and K. Dholakia, “Microfluidic sorting in an optical lattice,” Nature 426(6965), 421–424 (2003).
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Figures (7)

Fig. 1
Fig. 1 Enriched DAMO archaea culture (FISH image demonstrating that DAMO archaea typically form large clusters. Bioreactor microbial communities were hybridized with the DAMO archaea (Candidatus ‘Methanoperedens nitroreducens’) specific probe (S-*-Darch- 872-a-A-18 (5- GGCTCCACCCGTTGTAGT −3). Labeled cells were visualized on a confocal laser scanning microscope (Carl Zeiss, LSM512) with Ar-ion laser (488 nm) and two HeNe lasers (543 and 633 nm).
Fig. 2
Fig. 2 The microfluidic channel structure and schematic cell sorting procedure (black circles denote the target DAMO cells, rods or curved filaments represent non-target cells). The optical trap, shown in red, collects a target DAMO cell and translates it through the gap into the buffer. It is then taken significantly downstream for collection.
Fig. 3
Fig. 3 The key components of the experimental system. The laser beam passes through a series of relay optics and enters the objective, after which the it is focussed into the microfluidic chamber using a high-NA objective.
Fig. 4
Fig. 4 The schematic diagram of DAMO cultivation container with two compartments.
Fig. 5
Fig. 5 Images of the trapping and transfer the DAMO cell in the microfluidic chip. The DAMO cell is flowing in the main bacteria channel and is optically trapped (a and b). Then it is moved transversely from one side of the gap to the other, and then into the pure buffer solution (c-h). The spot at the bottom of (g) and (h) is likely to be PDMS detritus - it was present before the addition of buffer or bacteria.
Fig. 6
Fig. 6 Microscope images of DAMO archaea cells after 345 days of cultivation. DAMO archaea cells grow as irregular cocci 1-3 µm in diameter and are found as tetradococci-like or sarcina-like clusters. Scale bar = 1 µm. No other forms of bacteria were observed in the solution.
Fig. 7
Fig. 7 Methane accumulated consumption profile in the DAMO cultivation reactor.

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