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The Cell and the Sum of Its Parts: Patterns of Complexity in Biosignatures as Revealed by Deep UV Raman Spectroscopy

Sapers, Haley M. and Razzell Hollis, Joseph and Bhartia, Rohit and Beegle, Luther W. and Orphan, Victoria J. and Amend, Jan P. (2019) The Cell and the Sum of Its Parts: Patterns of Complexity in Biosignatures as Revealed by Deep UV Raman Spectroscopy. Frontiers in Microbiology, 10 . Art. No. 679. ISSN 1664-302X. https://resolver.caltech.edu/CaltechAUTHORS:20190530-074324675

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Abstract

The next NASA-led Mars mission (Mars 2020) will carry a suite of instrumentation dedicated to investigating Martian history and the in situ detection of potential biosignatures. SHERLOC, a deep UV Raman/Fluorescence spectrometer has the ability to detect and map the distribution of many organic compounds, including the aromatic molecules that are fundamental building blocks of life on Earth, at concentrations down to 1 ppm. The mere presence of organic compounds is not a biosignature: there is widespread distribution of reduced organic molecules in the Solar System. Life utilizes a select few of these molecules creating conspicuous enrichments of specific molecules that deviate from the distribution expected from purely abiotic processes. The detection of far from equilibrium concentrations of a specific subset of organic molecules, such as those uniquely enriched by biological processes, would comprise a universal biosignature independent of specific terrestrial biochemistry. The detectability and suitability of a small subset of organic molecules to adequately describe a living system is explored using the bacterium Escherichia coli as a model organism. The DUV Raman spectra of E. coli cells are dominated by the vibrational modes of the nucleobases adenine, guanine, cytosine, and thymine, and the aromatic amino acids tyrosine, tryptophan, and phenylalanine. We demonstrate that not only does the deep ultraviolet (DUV) Raman spectrum of E. coli reflect a distinct concentration of specific organic molecules, but that a sufficient molecular complexity is required to deconvolute the cellular spectrum. Furthermore, a linear combination of the DUV resonant compounds is insufficient to fully describe the cellular spectrum. The residual in the cellular spectrum indicates that DUV Raman spectroscopy enables differentiating between the presence of biomolecules and the complex uniquely biological organization and arrangements of these molecules in living systems. This study demonstrates the ability of DUV Raman spectroscopy to interrogate a complex biological system represented in a living cell, and differentiate between organic detection and a series of Raman features that derive from the molecular complexity inherent to life constituting a biosignature.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.3389/fmicb.2019.00679DOIArticle
ORCID:
AuthorORCID
Razzell Hollis, Joseph0000-0002-6239-694X
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2019 Sapers, Razzell Hollis, Bhartia, Beegle, Orphan and Amend. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. The U.S. Government retains a nonexclusive license to this work for non-commercial purposes. Received: 18 September 2018; Accepted: 18 March 2019; Published: 14 May 2019. Author Contributions: HS designed the study with significant input from JH, LB, and RB. HS cultured the cells, prepared the cell samples, and collected the cellular Raman spectra. HS and JH designed the analytical pipeline and wrote the processing code. JH made the standard solutions, collected the standard Raman spectra, and finalized the Raman analyses. HS and JH wrote the manuscript with significant input from RB and LB. JA and VO contributed to discussion, feasibility, and text. The work described in this paper was carried out at the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration. This work was funded by a NASA Astrobiology Institute–Life Underground (NAI-LU, NNA13AA92A) grant to JA, VO, and RB. Further support was provided by a Human Frontier Science Program postdoctoral fellowship to HS and a NASA Postdoctoral Program fellowship to JH. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank Nicholas Laughton and Kyle Uckert for valuable assistance with Python programming and William Abbey, Evan Eshelman, Greg Wanger, Michael Malaska, Ranjani Murali, Daan Speth, and Sean Mullin for insightful conversations and discussions regarding data analysis and data visualization.
Funders:
Funding AgencyGrant Number
NASA/JPL/CaltechUNSPECIFIED
NASANNA13AA92A
Human Frontier Science ProgramUNSPECIFIED
NASA Postdoctoral ProgramUNSPECIFIED
Subject Keywords:biosignatures, deep UV Raman spectroscopy, Mars 2020, SHERLOC, spectral deconvolution
Record Number:CaltechAUTHORS:20190530-074324675
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190530-074324675
Official Citation:Sapers HM, Razzell Hollis J, Bhartia R, Beegle LW, Orphan VJ and Amend JP (2019) The Cell and the Sum of Its Parts: Patterns of Complexity in Biosignatures as Revealed by Deep UV Raman Spectroscopy. Front. Microbiol. 10:679. doi: 10.3389/fmicb.2019.00679
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:95945
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:30 May 2019 16:26
Last Modified:03 Oct 2019 21:18

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