Imaging technologies and strategies for detection of extant extraterrestrial microorganisms

Abstract There is no reductionist definition of life, so the way organisms look, behave, and move is the most definitive way to identify extraterrestrial life. Life elsewhere in the Solar System is likely to be microbial, but no microscope capable of imaging prokaryotic life has ever flown on a lander mission to a habitable planet. Nonetheless, high-resolution microscopes have been developed that are appropriate for planetary exploration. Traditional light microscopy, interferometric microscopy, light-field microscopy, scanning probe microscopy, and electron microscopy are all possible techniques for the detection of extant micro-organisms on Mars and the moons of Jupiter and Saturn. This article begins with a general discussion of the challenges involved in searching for prokaryotic life, then reviews instruments that have flown, that have been selected for flight but not flown or not flown yet, and developing techniques of great promise for life detection that have not yet been selected for flight.

[1]  Edward H. Adelson,et al.  Single Lens Stereo with a Plenoptic Camera , 1992, IEEE Trans. Pattern Anal. Mach. Intell..

[2]  U. Schnars,et al.  Digital recording and numerical reconstruction of holograms: a new method for displaying light in flight. , 1995, Applied optics.

[3]  Changhuei Yang,et al.  Wide Field-of-view Fluorescence Image Deconvolution with Aberration-estimation from Fourier Ptychography References and Links , 2022 .

[4]  J. Bossa,et al.  Thermal reactions in interstellar ice: A step towards molecular complexity in the interstellar medium , 2013 .

[5]  Aydogan Ozcan,et al.  Wide-field computational color imaging using pixel super-resolved on-chip microscopy. , 2013, Optics express.

[6]  John Parnell,et al.  Raman spectroscopic analysis of geological and biogeological specimens of relevance to the ExoMars mission. , 2013, Astrobiology.

[7]  R. Stocker,et al.  Microbial Morphology and Motility as Biosignatures for Outer Planet Missions , 2016, Astrobiology.

[8]  Eugene Serabyn,et al.  A Mach-Zender digital holographic microscope with sub-micrometer resolution for imaging and tracking of marine micro-organisms. , 2014, The Review of scientific instruments.

[9]  E. Ford,et al.  Vegetation's red edge: a possible spectroscopic biosignature of extraterrestrial plants. , 2005, Astrobiology.

[10]  Michael A. Rice,et al.  The persistence of a chlorophyll spectral biosignature from Martian evaporite and spring analogues under Mars-like conditions , 2013, International Journal of Astrobiology.

[11]  Aydogan Ozcan,et al.  Lensfree color imaging on a nanostructured chip using compressive decoding. , 2010, Applied physics letters.

[12]  A. Gamal,et al.  Miniaturized integration of a fluorescence microscope , 2011, Nature Methods.

[13]  Manuel Bedrossian,et al.  Digital Holographic Microscopy, a Method for Detection of Microorganisms in Plume Samples from Enceladus and Other Icy Worlds , 2017, Astrobiology.

[14]  Aydogan Ozcan,et al.  Unconventional methods of imaging: computational microscopy and compact implementations , 2016, Reports on progress in physics. Physical Society.

[15]  N. I. Lewis,et al.  Swimming speed of three species of Alexandrium (Dinophyceae) as determined by digital in-line holography , 2006 .

[16]  J. Pratt,et al.  Use of fluorochromes for direct enumeration of total bacteria in environmental samples: past and present. , 1994, Microbiological reviews.

[17]  Christopher F Chyba,et al.  Clathrate hydrates of oxidants in the ice shell of Europa. , 2006, Astrobiology.

[18]  Manuel Bedrossian,et al.  A Submersible, Off-Axis Holographic Microscope for Detection of Microbial Motility and Morphology in Aqueous and Icy Environments , 2016, PloS one.

[19]  M. Fatih Toy,et al.  Enhanced robustness digital holographic microscopy for demanding environment of space biology , 2012, Biomedical optics express.

[20]  Noriaki Masui,et al.  Discriminative detection and enumeration of microbial life in marine subsurface sediments , 2009, The ISME Journal.

[21]  Andrew Packard,et al.  A system analysis approach for atmospheric observations and models: Mesospheric HOx dilemma , 2006 .

[22]  A. R. Sampson,et al.  Miniature Variable Pressure Scanning Electron Microscope for in-situ imaging & chemical analysis , 2012, 2012 IEEE Aerospace Conference.

[23]  V. Micó,et al.  Common-path phase-shifting digital holographic microscopy: A way to quantitative phase imaging and superresolution , 2008 .

[24]  Sun Kwok,et al.  Complex organics in space from Solar System to distant galaxies , 2016 .

[25]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[26]  Arnaud Belloche,et al.  Complex organic molecules in the interstellar medium: IRAM 30 m line survey of Sagittarius B2(N) and (M) , 2013, 1308.5062.

[27]  J. Gómez-Elvira,et al.  Underground habitats in the Río Tinto basin: a model for subsurface life habitats on Mars. , 2008, Astrobiology.

[28]  Reg G. Willson,et al.  Curiosity’s Mars Hand Lens Imager (MAHLI) Investigation , 2012 .

[29]  Colin Tudge,et al.  Planet , 1999 .

[30]  Joseph L. Kirschvink,et al.  Magnetofossils from Ancient Mars: a Robust Biosignature in the Martian Meteorite ALH84001 , 2002, Applied and Environmental Microbiology.

[31]  Jens Romstedt,et al.  MIDAS: Lessons learned from the first spaceborne atomic force microscope , 2016 .

[32]  M. D. Smith,et al.  Mineralogy at Meridiani Planum from the Mini-TES Experiment on the Opportunity Rover , 2004, Science.

[33]  Charles Cockell,et al.  New priorities in the robotic exploration of Mars: the case for in situ search for extant life. , 2010, Astrobiology.

[34]  Roland Siegwart,et al.  The ExoMars rover and Pasteur payload Phase A study: an approach to experimental astrobiology , 2006 .

[35]  Howell G. M. Edwards,et al.  Raman Spectroscopy of Microbial Pigments , 2014, Applied and Environmental Microbiology.

[36]  Pierre Bongrand,et al.  Synchronizing atomic force microscopy force mode and fluorescence microscopy in real time for immune cell stimulation and activation studies. , 2016, Ultramicroscopy.

[37]  Christopher F Chyba,et al.  Energy, chemical disequilibrium, and geological constraints on Europa. , 2007, Astrobiology.

[38]  Aydogan Ozcan,et al.  Color and monochrome lensless on-chip imaging of Caenorhabditis elegans over a wide field-of-view. , 2010, Lab on a chip.

[39]  Ericka Stricklin-Parker,et al.  Ann , 2005 .

[40]  Zach DeVito,et al.  Opt , 2017 .

[41]  Andrew Resnick,et al.  Multi-function Light Microscopy Module for the International Space Station , 2001 .

[42]  Pedro Cintas,et al.  On the physical basis of asymmetry and homochirality. , 2012, Chirality.

[43]  N. Streibl.  Depth Transfer by an Imaging System , 1984 .

[44]  D. Deamer,et al.  Lipids as universal biomarkers of extraterrestrial life. , 2014, Astrobiology.

[45]  R. Horstmeyer,et al.  Wide-field, high-resolution Fourier ptychographic microscopy , 2013, Nature Photonics.

[46]  Manfred H. Jericho,et al.  In-line digital holographic microscopy for terrestrial and exobiological research , 2010 .

[47]  Andro C. Rios,et al.  Enantiomer excesses of rare and common sugar derivatives in carbonaceous meteorites , 2016, Proceedings of the National Academy of Sciences.

[48]  Derek K. Tseng,et al.  Detection of waterborne parasites using field-portable and cost-effective lensfree microscopy. , 2010, Lab on a chip.

[49]  Christian Depeursinge,et al.  Simultaneous cell morphometry and refractive index measurement with dual-wavelength digital holographic microscopy and dye-enhanced dispersion of perfusion medium. , 2008, Optics letters.

[50]  Oliver Steinbock,et al.  Biomimetic mineral self-organization from silica-rich spring waters , 2017, Science Advances.

[51]  R. Olson,et al.  A submersible imaging‐in‐flow instrument to analyze nano‐and microplankton: Imaging FlowCytobot , 2007 .

[52]  A. McEwen,et al.  Transient liquid water and water activity at Gale crater on Mars , 2015 .

[53]  Tasnim Munshi,et al.  Destruction of Raman biosignatures by ionising radiation and the implications for life detection on Mars , 2012, Analytical and Bioanalytical Chemistry.

[54]  Yukishige Kawasaki,et al.  Direct detection of Martian microorganisms based on fluorescence microscopy , 1999 .

[55]  K. Tande,et al.  Capturing quantitative zooplankton information in the sea: Performance test of laser optical plankton counter and video plankton recorder in a Calanus finmarchicus dominated summer situation , 2013 .

[56]  Byongjun Hwang,et al.  Under-ice measurements of suspended particulate matters using ADCP and LISST-Holo , 2015, Ocean Science Journal.

[57]  Ian B. Hutchinson,et al.  Raman spectroscopy and the search for life signatures in the ExoMars Mission* , 2012, International Journal of Astrobiology.

[58]  Urs Staufer,et al.  Quantification of the dry history of the Martian soil inferred from in situ microscopy , 2011 .

[59]  Wolfgang Fink,et al.  Planetary imaging in powers of ten: a multiscale, multipurpose astrobiological imager. , 2013, Astrobiology.

[60]  Zeev Zalevsky,et al.  Superresolution digital holographic microscopy for three-dimensional samples. , 2008, Optics express.

[61]  A. Ozcan,et al.  Holographic pixel super-resolution in portable lensless on-chip microscopy using a fiber-optic array. , 2011, Lab on a chip.

[62]  Chun-Min Lo,et al.  High-resolution quantitative phase-contrast microscopy by digital holography. , 2005, Optics express.

[63]  Claire R. Cousins,et al.  Volcano-ice interaction: a haven for life on Mars? , 2011 .

[64]  Frances Westall,et al.  Testing the ability of the ExoMars 2018 payload to document geological context and potential habitability on Mars , 2015 .

[65]  J. Bibring,et al.  Micromega/IR: Design and status of a near-infrared spectral microscope for in situ analysis of Mars samples , 2009 .

[66]  Roberto Furfaro,et al.  The Biological Oxidant and Life Detection (BOLD) mission: A proposal for a mission to Mars , 2012 .

[67]  José Antonio Rodríguez Manfredi,et al.  Strategies for detection of putative life on Europa , 2011 .

[68]  Nicolas Thomas,et al.  The microscope for Beagle 2 , 2004 .

[69]  Antonio Quesada,et al.  Critical Assessment of Analytical Techniques in the Search for Biomarkers on Mars: A Mummified Microbial Mat from Antarctica as a Best-Case Scenario , 2017, Astrobiology.

[70]  Charles S Cockell,et al.  Fourier Transform Infrared Spectral Detection of Life in Polar Subsurface Environments and its Application to Mars Exploration , 2015, Applied spectroscopy.

[71]  Gilbert V. Levin,et al.  Complexity Analysis of the Viking Labeled Release Experiments , 2012 .

[72]  N. Streibl.  Three-dimensional imaging by a microscope , 1985 .

[73]  Chris McKay,et al.  What Is Life—and How Do We Search for It in Other Worlds? , 2004, PLoS biology.

[74]  Nicolas Thomas,et al.  An efficient autofocus algorithm for a visible microscope on a Mars lander , 2010 .

[75]  Jonas Kühn,et al.  Improved Tracking and Resolution of Bacteria in Holographic Microscopy Using Dye and Fluorescent Protein Labeling , 2016, Front. Chem..

[76]  Yibo Zhang,et al.  Color calibration and fusion of lens-free and mobile-phone microscopy images for high-resolution and accurate color reproduction , 2016, Scientific Reports.

[77]  Gregg A Swayze,et al.  Science applications of a multispectral microscopic imager for the astrobiological exploration of Mars. , 2014, Astrobiology.

[78]  Andrew G. Glen,et al.  APPL , 2001 .

[79]  R Riesenberg,et al.  Reconstruction of high-resolution holographic microscopic images. , 2009, Optics letters.

[80]  G. Manzini,et al.  Interaction of diamidino-2-phenylindole (DAPI) with natural and synthetic nucleic acids. , 1983, Nucleic acids research.

[81]  Jianglai Wu,et al.  A light sheet based high throughput 3D-imaging flow cytometer for phytoplankton analysis. , 2013, Optics express.

[82]  Didier Beghuin,et al.  Invited review article: Advanced light microscopy for biological space research. , 2014, The Review of scientific instruments.

[83]  Matthew Gunn,et al.  Mars surface context cameras past, present, and future , 2016 .

[84]  E. Cuche,et al.  Measurement of the integral refractive index and dynamic cell morphometry of living cells with digital holographic microscopy. , 2005, Optics express.

[85]  E. Cuche,et al.  Digital holographic microscopy: a noninvasive contrast imaging technique allowing quantitative visualization of living cells with subwavelength axial accuracy. , 2005, Optics letters.

[86]  Paul D. Feldman,et al.  The search for a subsurface ocean in Ganymede with Hubble Space Telescope observations of its auroral ovals , 2015 .

[87]  Edward W. Schwieterman,et al.  Nonphotosynthetic Pigments as Potential Biosignatures , 2014, Astrobiology.

[88]  Daniel Buscombe,et al.  Evaluating Unsupervised Methods to Size and Classify Suspended Particles Using Digital In-Line Holography , 2015 .

[89]  Kristina Haase,et al.  Investigating cell mechanics with atomic force microscopy , 2015, Journal of The Royal Society Interface.

[90]  Gilbert V Levin,et al.  The Case for Extant Life on Mars and Its Possible Detection by the Viking Labeled Release Experiment. , 2016, Astrobiology.

[91]  G. Klingelhöfer,et al.  Identification of morphological biosignatures in Martian analogue field specimens using in situ planetary instrumentation. , 2008, Astrobiology.

[92]  Pradeep Kumar,et al.  Survivability and growth kinetics of methanogenic archaea at various pHs and pressures: Implications for deep subsurface life on Mars , 2017 .

[93]  C Knox,et al.  Holographic Microscopy as a Technique for Recording Dynamic Microscopic Subjects , 1966, Science.

[94]  K. Porter,et al.  The use of DAPI for identifying and counting aquatic microflora1 , 1980 .

[95]  Joseph Rosen,et al.  In-line FINCH super resolution digital holographic fluorescence microscopy using a high efficiency transmission liquid crystal GRIN lens. , 2013, Optics letters.

[96]  Kenneth S. Edgett,et al.  MAHLI on Mars: lessons learned operating a geoscience camera on a landed payload robotic arm , 2016 .

[97]  Jae-Hyeung Park,et al.  Super-resolution digital holographic microscopy using multi-point light sources illumination , 2010, OPTO.

[98]  J. Deming,et al.  A microscopic approach to investigate bacteria under in situ conditions in sea-ice samples , 2001, Annals of Glaciology.

[99]  T. Lowenstein,et al.  Identification of carotenoids in ancient salt from Death Valley, Saline Valley, and Searles Lake, California, using laser Raman spectroscopy. , 2012, Astrobiology.

[100]  Ronen Basri,et al.  Separation of Transparent Layers using Focus , 2004, International Journal of Computer Vision.

[101]  Eugene Serabyn,et al.  Robust, compact implementation of an off-axis digital holographic microscope. , 2015, Optics express.