Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-27T23:09:32.021Z Has data issue: false hasContentIssue false
  • English
  • Français

The non-destructive separation of diverse astrobiologically relevant organic molecules by customizable capillary zone electrophoresis and monolithic capillary electrochromatography

Published online by Cambridge University Press:  29 May 2019

Kosuke Fujishima Open the ORCID record for Kosuke Fujishima [Opens in a new window] ,
Szymon Dziomba ,
Hajime Yano ,
Seydina I. Kebe ,
Mohamed Guerrouache ,
Benjamin Carbonnier  and
Lynn J. Rothschild
Kosuke Fujishima
Affiliation:
Earth-Life Science Institute, Tokyo Institute of Technology, Tokyo 1528550, Japan Universities Space Research Association at NASA Ames Research Center, Moffett Field, CA 94035, USA
Szymon Dziomba
Affiliation:
Université Paris-Est, UPEC, ICMPE (UMR7182), 94320, Thiais, France Department of Toxicology, Faculty of Pharmacy, Medical University of Gdansk, 107 Hallera Street, 80-416 Gdansk, Poland
Hajime Yano
Affiliation:
Institute of Space and Astronautical Science (ISAS), Japan Aerospace Exploration Agency (JAXA), 3-1-1 Yoshinodai, Chuo-ku, Sagamihara 252-5210, Japan
Seydina I. Kebe
Affiliation:
Université Paris-Est, UPEC, ICMPE (UMR7182), 94320, Thiais, France
Mohamed Guerrouache
Affiliation:
Université Paris-Est, UPEC, ICMPE (UMR7182), 94320, Thiais, France
Benjamin Carbonnier*
Affiliation:
Université Paris-Est, UPEC, ICMPE (UMR7182), 94320, Thiais, France
Lynn J. Rothschild*
Affiliation:
NASA Ames Research Center, Moffett Field, CA 94035, USA
*
Author for correspondence: Lynn J. Rothschild, E-mail: [email protected] and Benjamin Carbonnier, E-mail: [email protected]
Author for correspondence: Lynn J. Rothschild, E-mail: [email protected] and Benjamin Carbonnier, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The in situ detection of organic molecules in space is key to understanding the variety and the distribution of the building blocks of life, and possibly the detection of extraterrestrial life itself. Gas chromatography mass spectrometry (GC-MS) has been the most sensitive analytical strategy for organic analyses in flight, and was used on missions from NASA's Viking, Phoenix, Curiosity missions to ESA's Rosetta space probe. While pyrolysis GC-MS revealed the first organics on Mars, this step alters or degrades certain fragile molecules that are excellent biosignatures including polypeptides, oligonucleotides and polysaccharides, rendering the intact precursors undetectable. We have identified a solution tailored to the detection of biopolymers and other biomarkers by the use of liquid-based capillary electrophoresis and electrochromatography. In this study, we show that a capillary electrochromatography approach using monolithic stationary phases with tailor-made surface chemistry can separate and identify various polycyclic aromatic hydrocarbons, nucleobases and aromatic acids that could be formed under astrophysically relevant conditions. In order to simulate flyby organic sample capture, we conducted hypervelocity impact experiments which consisted of accelerating peptide-soaked montmorillonite particles to a speed of 5.6 km s−1, and capturing them in an amorphous silica aerogel of 10 mg cm−3 bulk density. Bulk peptide extraction from aerogel followed by capillary zone electrophoresis led to the detection of only two stereoisomeric peptide peaks. The recovery rates of each step of the extraction procedure after the hypervelocity impact suggest that major peptide loss occurred during the impact. Our study provides initial exploration of feasibility of this approach for capturing intact peptides, and subsequently detecting candidate biomolecules during flight missions that would be missed by GC-MS alone. As the monolith-based electrochromatography technology could be customized to detect specific classes of compounds as well as miniaturized, these results demonstrate the potential of the instrumentation for future astrobiology-related spaceflight missions.

Keywords

Aerogelastrobiologybiosignaturecapillary zone electrophoresiselectrochromatographyflight instrumentflyby sample returnmonolithic capillary
Type
Research Article
Information
International Journal of Astrobiology , Volume 18 , Issue 6 , December 2019 , pp. 562 - 574
Creative Commons
This is a work of the U.S. Government and is not subject to copyright protection in the United States.
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Contributed equally.

References

Akbay, C, Shamsi, SA and Warner, IM (1997) Phosphated surfactants as pseudostationary phase for micellar electrokinetic chromatography: separation of polycyclic aromatic hydrocarbons. Electrophoresis 18, 253–259.Google Scholar
Ali, I, Al-Othman, ZA, Al-Warthan, A, Asnin, L and Chudinov, A (2014) Advances in chiral separations of small peptides by capillary electrophoresis and chromatography. Journal of Separation Science 37, 2447–2466.Google Scholar
Alpert, AJ (1990) Hydrophilic-interaction chromatography for the separation of peptides, nucleic acids and other polar compounds. Journal of Chromatography 499, 177–196.Google Scholar
Aubrey, AD, Chalmers, JH, Bada, JL, Grunthaner, FJ, Amashukeli, X, Willis, P, Skelley, AM, Mathies, RA, Quinn, RC, Zent, AP, Ehrenfreund, P, Amundson, R, Glavin, DP, Botta, O, Barron, L, Blaney, DL, Clark, BC, Coleman, M, Hofmann, BA, Josset, JL, Rettberg, P, Ride, S, Robert, F, Sephton, MA and Yen, A (2008) The Urey instrument: an advanced in situ organic and oxidant detector for Mars exploration. Astrobiology 8, 583–595.Google Scholar
Barrett, RA, Zolensky, ME, Horz, F, Lindstrom, DJ and Gibson, EK (1992) Suitability of silica aerogel as a capture medium for interplanetary dust. Proceedings, 22nd Lunar and Planetary Science 22, 203–212.Google Scholar
Belloche, A, Muller, HSP, Menten, KM, Schilke, P and Comito, C (2013) Complex organic molecules in the interstellar medium: IRAM 30 m line survey of Sagittarius B2(N) and (M). Astronomy and Astrophysics 559(A47), 1–187.Google Scholar
Brownlee, DE, Hörz, F, Hrubsh, L, McDonnell, JAM, Tsou, P and Williams, J (1994) Eureka! Aerogel capture of meteoroids in space. Abstracts, Lunar and Planetary Science Conference, 183–184.Google Scholar
Brownlee, D, Tsou, P, Aléon, J, Alexander, CM, Araki, T, Bajt, S, Baratta, GA, Bastien, R, Bland, P, Bleuet, P, Borg, J, Bradley, JP, Brearley, A, Brenker, F, Brennan, S, Bridges, JC, Browning, ND, Brucato, JR, Bullock, E, Burchell, MJ, Busemann, H, Butterworth, A, Chaussidon, M, Cheuvront, A, Chi, M, Cintala, MJ, Clark, BC, Clemett, SJ, Cody, G, Colangeli, L, Cooper, G, Cordier, P, Daghlian, C, Dai, Z, D'Hendecourt, L, Djouadi, Z, Dominguez, G, Duxbury, T, Dworkin, JP, Ebel, DS, Economou, TE, Fakra, S, Fairey, SA, Fallon, S, Ferrini, G, Ferroir, T, Fleckenstein, H, Floss, C, Flynn, G, Franchi, IA, Fries, M, Gainsforth, Z, Gallien, JP, Genge, M, Gilles, MK, Gillet, P, Gilmour, J, Glavin, DP, Gounelle, M, Grady, MM, Graham, GA, Grant, PG, Green, SF, Grossemy, F, Grossman, L, Grossman, JN, Guan, Y, Hagiya, K, Harvey, R, Heck, P, Herzog, GF, Hoppe, P, Hörz, F, Huth, J, Hutcheon, ID, Ignatyev, K, Ishii, H, Ito, M, Jacob, D, Jacobsen, C, Jacobsen, S, Jones, S, Joswiak, D, Jurewicz, A, Kearsley, AT, Keller, LP, Khodja, H, Kilcoyne, AL, Kissel, J, Krot, A, Langenhorst, F, Lanzirotti, A, Le, L, Leshin, LA, Leitner, J, Lemelle, L, Leroux, H, Liu, MC, Luening, K, Lyon, I, Macpherson, G, Marcus, MA, Marhas, K, Marty, B, Matrajt, G, McKeegan, K, Meibom, A, Mennella, V, Messenger, K, Messenger, S, Mikouchi, T, Mostefaoui, S, Nakamura, T, Nakano, T, Newville, M, Nittler, LR, Ohnishi, I, Ohsumi, K, Okudaira, K, Papanastassiou, DA, Palma, R, Palumbo, ME, Pepin, RO, Perkins, D, Perronnet, M, Pianetta, P, Rao, W, Rietmeijer, FJ, Robert, F, Rost, D, Rotundi, A, Ryan, R, Sandford, SA, Schwandt, CS, See, TH, Schlutter, D, Sheffield-Parker, J, Simionovici, A, Simon, S, Sitnitsky, I, Snead, CJ, Spencer, MK, Stadermann, FJ, Steele, A, Stephan, T, Stroud, R, Susini, J, Sutton, SR, Suzuki, Y, Taheri, M, Taylor, S, Teslich, N, Tomeoka, K, Tomioka, N, Toppani, A, Trigo-Rodríguez, JM, Troadec, D, Tsuchiyama, A, Tuzzolino, AJ, Tyliszczak, T, Uesugi, K, Velbel, M, Vellenga, J, Vicenzi, E, Vincze, L, Warren, J, Weber, I, Weisberg, M, Westphal, AJ, Wirick, S, Wooden, D, Wopenka, B, Wozniakiewicz, P, Wright, I, Yabuta, H, Yano, H, Young, ED, Zare, RN, Zega, T, Ziegler, K, Zimmerman, L, Zinner, E and Zolensky, M (2006) Comet 81P/Wild 2 under a microscope. Science 314, 1711–1716.Google Scholar
Burchell, MJ, Thomson, R and Yano, H (1998) Capture of hypervelocity particles in aerogel: in ground laboratory and low earth orbit. Planetary and Space Science 47, 189–204.Google Scholar
Burchell, MJ, Foster, NJ, Ormond Prout, J, Dupin, D and Armes, SP (2009) Extent of thermal ablation suffered by model organic microparticles during aerogel capture at hypervelocities. Meteoritics & Planetary Science 44, 1407–1419.Google Scholar
Burchell, MJ, Cole, MJ, Price, MC, Kearsley, AT and Nixon, A (2010) Glycine survival in hypervelocity impacts in the laboratory into aerogel and onto aluminium foil. Lunar and Planetary Science Conference 41, 1637.Google Scholar
Burchell, MJ, Bowden, SA, Cole, M, Price, MC and Parnell, J (2014) Survival of organic materials in hypervelocity impacts of ice on sand, ice, and water in the laboratory. Astrobiology 14, 473–485.Google Scholar
Burgi, DS and Chien, RL (1991) Optimization in sample stacking for high-performance capillary electrophoresis. Analytical Chemistry 63, 2042–2047.Google Scholar
Callahan, MP, Smith, KE, Cleaves, HJ, Ruzicka, J, Stern, JC, Glavin, DP, House, CH and Dworkin, JP (2011) Carbonaceous meteorites contain a wide range of extraterrestrial nucleobases. Proceedings of the National Academy of Sciences of the United States of America 108, 13995–13998.Google Scholar
Carbonnier, B, Guerrouache, M, Denoyel, R and Millot, MC (2007) CEC separation of aromatic compounds and proteins on hexylamine-functionalized N-acryloxysuccinimide monoliths. Journal of Separation Science 30, 3000–3010.Google Scholar
Chen, JH, Shi, Q, Wang, YL, Li, ZY and Wang, S (2015) Dereplication of known nucleobase and nucleoside compounds in natural product extracts by capillary electrophoresis-high resolution mass spectrometry. Molecules 20, 5423–5437.Google Scholar
Cooper, G and Rios, AC (2016) Enantiomer excesses of rare and common sugar derivatives in carbonaceous meteorites. Proceedings of the National Academy of Sciences of the United States of America 113, E3322–E3331.Google Scholar
Cooper, G, Reed, C, Nguyen, D, Carter, M and Wang, Y (2011) Detection and formation scenario of citric acid, pyruvic acid, and other possible metabolism precursors in carbonaceous meteorites. Proceedings of the National Academy of Sciences of the United States of America 108, 14015–14020.Google Scholar
Coussot, G, Moreau, T, Faye, C, Vigier, F, Baqué, M, Le Postollec, A, Incerti, S, Dobrijevic, M and Vandenabeele-Trambouze, O (2017) Biochip-based instruments development for space exploration: influence of the antibody immobilization process on the biochip resistance to freeze-drying, temperature shifts and cosmic radiations. International Journal of Astrobiology 16, 190–199.Google Scholar
Creamer, JS, Mora, MF and Willis, PA (2017) Enhanced resolution of chiral amino acids with capillary electrophoresis for biosignature detection in extraterrestrial samples. Analytical Chemistry 89, 1329–1337.Google Scholar
Domínguez, G (2009) Time evolution and temperatures of hypervelocity impact-generated tracks in aerogel. Meteoritics & Planetary Science 44, 1431–1443.Google Scholar
Dziomba, S, Kowalski, P, Slominska, A and Baczek, T (2014) Field-amplified sample injection coupled with pseudo-isotachophoresis technique for sensitive determination of selected psychiatric drugs in human urine samples after dispersive liquid-liquid microextraction. Analytica Chimica Acta 811, 88–93.Google Scholar
Ehrenfreund, P, Rasmussen, S, Cleaves, J and Chen, L (2006) Experimentally tracing the key steps in the origin of life: the aromatic world. Astrobiology 6, 490–520.Google Scholar
Elsila, JE, Glavin, DP and Dworkin, JP (2009) Cometary glycine detected in samples returned by Stardust. Meteoritics & Planetary Science 44, 1323–1330.Google Scholar
Engel, MH and Macko, SA (1997) Isotopic evidence for extraterrestrial non-racemic amino acids in the Murchison meteorite. Nature 389, 265–268.Google Scholar
Glavin, DP, Callahan, MP, Dworkin, JP and Elsila, JE (2010) The effects of parent body processes on amino acids in carbonaceous chondrites. Meteoritics & Planetary Science 45, 1948–1972.Google Scholar
Guerrouache, M, Carbonnier, B, Vidal-Madjar, C and Millot, MC (2007) In situ functionalization of N-acryloxysuccinimide-based monolith for reversed-phase electrochromatography. Journal of Chromatography A 1149, 368–376.Google Scholar
Guerrouache, M, Millot, M-C and Carbonnier, B (2009) Functionalization of macroporous organic polymer monolith based on succinimide ester reactivity for chiral capillary chromatography: a cyclodextrin click approach. Macromolecular Rapid Communications 30, 109–113.Google Scholar
Guerrouache, M, Millot, MC and Carbonnier, B (2011) Capillary columns for reversed-phase CEC prepared via surface functionalization of polymer monolith with aromatic selectors. Journal of Separation Science 34, 2271–2278.Google Scholar
Guo, S, Duan, JA, Qian, D, Wang, H, Tang, Y, Qian, Y, Wu, D, Su, S and Shang, E (2013) Hydrophilic interaction ultra-high performance liquid chromatography coupled with triple quadrupole mass spectrometry for determination of nucleotides, nucleosides and nucleobases in Ziziphus plants. Journal of Chromatography A 1301, 147–155.Google Scholar
Hiller, DA and Strobel, SA (2011) The chemical versatility of RNA. Philosophical Transactions of the Royal Society of London B Biological Sciences 366, 2929–2935.Google Scholar
Hörz, F and Zolensky, ME (2000) Impact features and projectile residues in aerogel exposed on Mir. Icarus 147, 559–579.Google Scholar
Hörz, F, Cintala, MJ, Zolensky, ME, Bernhard, RB, Davidson, WE, Haynes, G, See, TH, Tsou, P and Brownlee, DE (1998) Capture of hypervelocity particles with low-density aerogel. NASA Technical Memorandum 98, 1–59.Google Scholar
Hörz, F, Cintala, MJ, See, TH and Messenger, KN (2009) Penetration tracks in aerogel produced by Al2O3 spheres. Meteoritics & Planetary Science 44, 1243–1264.Google Scholar
Jung, SH and Choe, JC (2013) Mechanisms of prebiotic adenine synthesis from HCN by oligomerization in the gas phase. Astrobiology 13, 465–475.Google Scholar
Kaiser, RI, Stockton, AM, Kim, YS, Jensen, EC and Mathies, RA (2013) On the formation of dipeptides in interstellar model ices. The Astrophysical Journal 765, 111.Google Scholar
Kasicka, V (1999) Capillary electrophoresis of peptides. Electrophoresis 20, 3084–3105.Google Scholar
Kasicka, V (2006) Recent developments in capillary electrophoresis and capillary electrochromatography of peptides. Electrophoresis 27, 142–175.Google Scholar
Kim, J, Jensen, EC, Stockton, AM and Mathies, RA (2013) Universal microfluidic automaton for autonomous sample processing: application to the Mars organic analyzer. Analytical Chemistry 85, 7682–7688.Google Scholar
Kitazawa, Y, Fujiwara, A, Kadono, T, Imagawa, K, Okada, Y and Uematsu, K (1999) Hypervelocity impact experiments on aerogel dust collector. Journal of Geophysical Research: Planets 104, 22035–22052.Google Scholar
Lerner, NR, Peterson, E and Chang, S (1993) The Strecker synthesis as a source of amino-acids in carbonaceous chondrites - deuterium retention during synthesis. Geochimica et Cosmochimica Acta 57, 4713–4723.Google Scholar
Marrubini, G, Mendoza, BE and Massolini, G (2010) Separation of purine and pyrimidine bases and nucleosides by hydrophilic interaction chromatography. Journal of Separation Science 33, 803–816.Google Scholar
Mathies, RA, Razu, ME, Kim, J, Stockton, AM, Turin, P and Butterworth, A (2017) Feasibility of detecting bioorganic compounds in Enceladus plumes with the Enceladus organic analyzer. Astrobiology 17, 902–912.Google Scholar
Mita, H, Yamagishi, A, Yano, H, Okudaira, K, Kobayashi, K, Yokobori, SI, Tabata, M, Kawai, H, Hashimoto, H and Wg, T (2009) TANPOPO: astrobiology exposure and micrometeoroid capture experiments on the KIBO, ISS. Origins of Life and Evolution of Biospheres 39, 371–372.Google Scholar
Mora, MF, Stockton, AM and Willis, PA (2012) Microchip capillary electrophoresis instrumentation for in situ analysis in the search for extraterrestrial life. Electrophoresis 33, 2624–2638.Google Scholar
Mora, MF, Jones, SM, Creamer, J and Willis, PA (2018) Extraction of amino acids from aerogel for analysis by capillary electrophoresis. Implications for a mission concept to Enceladus’ Plume. Electrophoresis 39, 620–625.Google Scholar
Mousis, O, Lunine, JI, Waite, JH, Magee, B, Lewis, WS, Mandt, KE, Marquer, D and Cordier, D (2009) Formation conditions of Enceladus and origin of its methane reservoir. The Astrophysical Journal. Letters 701, L39–L42.Google Scholar
Nixon, A, Burchell, MJ, Price, MC, Kearsley, AT and Jones, S (2012) Aerogel tracks made by impacts of glycine: implications for formation of bulbous tracks in aerogel and the Stardust mission. Meteoritics & Planetary Science 47, 623–633.Google Scholar
Okudaira, K, Noguchi, T, Nakamura, T, Sugita, S, Sekine, Y and Yano, H (2004) Evaluation of mineralogical alteration of micrometeoroid analog materials captured in aerogel. Advances in Space Research 34, 2299–2304.Google Scholar
Patel, BH, Percivalle, C, Ritson, DJ, Duffy, CD and Sutherland, JD (2015) Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nature Chemistry 7, 301–307.Google Scholar
Pizzarello, S (2006) The chemistry of life's origin: a carbonaceous meteorite perspective. Accounts of Chemical Research 39, 231–237.Google Scholar
Poinot, P and Geffroy-Rodier, C (2015) Searching for organic compounds in the Universe. TrAC-Trends in Analytical Chemistry 65, 1–12.Google Scholar
Powner, MW, Gerland, B and Sutherland, JD (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242.Google Scholar
Quirino, JP and Terabe, S (2000) Sample stacking of cationic and anionic analytes in capillary electrophoresis. Journal of Chromatography A 902, 119–135.Google Scholar
Rix, CS, Sims, MR and Cullen, DC (2011) Immunological detection of small organic molecules in the presence of perchlorates: relevance to the life marker chip and life detection on Mars. Astrobiology 11, 839–846.Google Scholar
Sandford, SA, Aléon, J, Alexander, CM, Araki, T, Bajt, S, Baratta, GA, Borg, J, Bradley, JP, Brownlee, DE, Brucato, JR, Burchell, MJ, Busemann, H, Butterworth, A, Clemett, SJ, Cody, G, Colangeli, L, Cooper, G, D'Hendecourt, L, Djouadi, Z, Dworkin, JP, Ferrini, G, Fleckenstein, H, Flynn, GJ, Franchi, IA, Fries, M, Gilles, MK, Glavin, DP, Gounelle, M, Grossemy, F, Jacobsen, C, Keller, LP, Kilcoyne, AL, Leitner, J, Matrajt, G, Meibom, A, Mennella, V, Mostefaoui, S, Nittler, LR, Palumbo, ME, Papanastassiou, DA, Robert, F, Rotundi, A, Snead, CJ, Spencer, MK, Stadermann, FJ, Steele, A, Stephan, T, Tsou, P, Tyliszczak, T, Westphal, AJ, Wirick, S, Wopenka, B, Yabuta, H, Zare, RN and Zolensky, ME (2006) Organics captured from comet 81P/Wild 2 by the stardust spacecraft. Science 314, 1720–1724.Google Scholar
Schmitt-Kopplin, P, Gabelica, Z, Gougeon, RD, Fekete, A, Kanawati, B, Harir, M, Gebefuegi, I, Eckel, G and Hertkorn, N (2010) High molecular diversity of extraterrestrial organic matter in Murchison meteorite revealed 40 years after its fall. Proceedings of the National Academy of Sciences of the United States of America 107, 2763–2768.Google Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.Google Scholar
Scriba, GKE (2006) Recent advances in peptide and peptidomimetic stereoisomer separations by capillary electromigration techniques. Electrophoresis 27, 222–230.Google Scholar
Scriba, GKE (2009) Recent developments in peptide stereoisomer separations by capillary electromigration techniques. Electrophoresis 30, S222–S228.Google Scholar
Sekine, Y, Takano, Y, Yano, H, Funase, R, Takai, K, Ishihara, M, Shibuya, T, Tachibana, S, Kuramoto, K, Yabuta, H, Kimura, J and Furukawa, Y (2014) Exploration of Enceladus’ water-rich plumes toward understanding of chemistry and biology of the interior ocean. Aerospace Technology Japan 12, Tk_7–Tk_11.Google Scholar
Sephton, MA and Botta, O (2008) Extraterrestrial organic matter and the detection of life. Space Science Reviews 135, 25–35.Google Scholar
Spencer, MK, Clemett, SJ, Sandford, SA, Mckay, DS and Zare, RN (2009) Organic compound alteration during hypervelocity collection of carbonaceous materials in aerogel. Meteoritics & Planetary Science 44, 15–24.Google Scholar
Stockton, AM, Chiesl, TN, Scherer, JR and Mathies, RA (2009) Polycyclic aromatic hydrocarbon analysis with the Mars organic analyzer microchip capillary electrophoresis system. Analytical Chemistry 81, 790–796.Google Scholar
Sugahara, H and Mimura, K (2015) Peptide synthesis triggered by comet impacts: a possible method for peptide delivery to the early Earth and icy satellites. Icarus 257, 103–112.Google Scholar
Summons, RE, Albrecht, P, McDonald, G and Moldowan, JM (2007) Molecular biosignatures. Space Science Reviews 135, 133–159.Google Scholar
Tabata, M, Yano, H, Kawai, H, Imai, E, Kawaguchi, Y, Hashimoto, H and Yamagishi, A (2015) Silica aerogel for capturing intact interplanetary dust particles for the Tanpopo experiment. Origins of Life and Evolution Biospheres 45, 225–229.Google Scholar
Tielens, AGGM (2008) Interstellar polycyclic aromatic hydrocarbon molecules. Annual Review of Astronomy and Astrophysics 46, 289–337.Google Scholar
Tsou, P, Brownlee, DE, Sandford, SA, Hörz, F and Zolensky, ME (2003) Wild 2 and interstellar sample collection and Earth return. Journal of Geophysical Research: Planets 108(E10).Google Scholar
Westphal, AJ, Snead, C, Borg, J, Quirico, E, Raynal, PI, Zolensky, ME, Ferrini, G, Colangeli, L and Palumbo, P (2002) Small hypervelocity particles captured in aerogel collectors: location, extraction, handling and storage. Meteoritics & Planetary Science 37, 855–865.Google Scholar
Westphal, AJ, Snead, C, Butterworth, A, Graham, GA, Bradley, JP, Bajt, S, Grant, PG, Bench, G, Brennan, S and Pianetta, P (2004) Aerogel keystones: extraction of complete hypervelocity impact events from aerogel collectors. Meteoritics & Planetary Science 39, 1375–1386.Google Scholar
Willis, PA, Creamer, JS and Mora, MF (2015) Implementation of microchip electrophoresis instrumentation for future spaceflight missions. Analytical and Bioanalytical Chemistry 407, 6939–6963.Google Scholar
Yabuta, H, Williams, LB, Cody, GD, Alexander, CMO and Pizzarello, S (2007) The insoluble carbonaceous material of CM chondrites: a possible source of discrete organic compounds under hydrothermal conditions. Meteoritics & Planetary Science 42, 37–48.Google Scholar
Yano, H, Yamagishi, A, Hashimoto, H, Yokobori, S, Kebukawa, Y, Kawaguchi, Y, Kobayashi, K, Yabuta, H, Tabata, M and Higashide, M (2015) Tanpopo: a New micrometeoroid capture and astrobiology exposure in Leo: its first year operation and post-flight plan. 78th Annual Meeting of the Meteoritical Society 1856, 5395.Google Scholar
Zhang, CX and Thormann, W (1996) Head-column field-amplified sample stacking in binary system capillary electrophoresis: a robust approach providing over 1000-fold sensitivity enhancement. Analytical Chemistry 68, 2523–2532.Google Scholar