4
The Potential for Finding Biosignatures in Returned Martian Samples

Over the past decade, growth in the field of geomicrobiology has significantly advanced understanding of the varied roles that microorganisms play in sedimentary processes and has helped define new approaches for the astrobiological exploration of Mars.1,2 Specifically, studies in a wide variety of modern and ancient environments on Earth have shown that microbial biosignatures (both chemical and morphological) are commonly and preferentially preserved in certain types of sedimentary deposits. Many of these terrestrial examples have relevance for Mars, because similar environments and processes are thought to have operated there earlier in the planet’s history. Of special interest for Mars sample return are the deposits of chemical sedimentary environments, like mineralizing springs and seeps, evaporitive lakes, and sites of fine-grained (e.g., phyllosilicate-rich) sedimentation,3 that have recently been discovered on Mars and are regarded as important potential sites for future landed missions and possibly sample return. On Earth, the above environments typically provide highly favorable nutrient and energy conditions for the growth and reproduction of organisms. In addition, such environments often provide contemporaneously high rates of mineral precipitation, which favors the formation of protective mineral coatings that can enhance the long-term viability of organisms entombed within minerals and increase their potential for preservation as fossil biosignatures.

The question naturally arises in the context of planetary protection, Why care about long-dead fossil biosignatures? If geological samples are returned from Mars, fossils will pose no hazards and therefore can be ignored for purposes of planetary protection. However, there are sound reasons to want to understand the signatures of life found in ancient geological materials. First, it has now been established with reasonable certainty that some types of microorganisms entombed in aqueous minerals and ices can maintain viability for prolonged spans of time (millions to possibly hundreds of millions of years; see examples cited below). Second, the initial characterization of returned martian samples contained within a sample-receiving facility (Chapters 6 and 7), which will be used to guide subsampling for biohazard testing and to inform decisions about sample allocations for further testing, or release from containment, will require understanding of the nature and origin of any organic matter present, whether derived from inorganic sources, from living or dormant life forms, or from fossils. For these reasons, it is prudent to briefly review some of the studies of biosignature capture and preservation that have been carried out in relevant terrestrial environments over the past decade. The number of published studies is substantial, and only a brief review of examples is provided here.



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4 The Potential for Finding Biosignatures in Returned Martian Samples Over the past decade, growth in the field of geomicrobiology has significantly advanced understanding of the varied roles that microorganisms play in sedimentary processes and has helped define new approaches for the astrobiological exploration of Mars.1,2 Specifically, studies in a wide variety of modern and ancient environments on Earth have shown that microbial biosignatures (both chemical and morphological) are commonly and pref- erentially preserved in certain types of sedimentary deposits. Many of these terrestrial examples have relevance for Mars, because similar environments and processes are thought to have operated there earlier in the planet’s history. Of special interest for Mars sample return are the deposits of chemical sedimentary environments, like mineralizing springs and seeps, evaporitive lakes, and sites of fine-grained (e.g., phyllosilicate-rich) sedimenta- tion,3 that have recently been discovered on Mars and are regarded as important potential sites for future landed missions and possibly sample return. On Earth, the above environments typically provide highly favorable nutrient and energy conditions for the growth and reproduction of organisms. In addition, such environments often provide contemporaneously high rates of mineral precipitation, which favors the formation of protective mineral coatings that can enhance the long-term viability of organisms entombed within minerals and increase their potential for preservation as fossil biosignatures. The question naturally arises in the context of planetary protection, Why care about long-dead fossil biosig- natures? If geological samples are returned from Mars, fossils will pose no hazards and therefore can be ignored for purposes of planetary protection. However, there are sound reasons to want to understand the signatures of life found in ancient geological materials. First, it has now been established with reasonable certainty that some types of microorganisms entombed in aqueous minerals and ices can maintain viability for prolonged spans of time (millions to possibly hundreds of millions of years; see examples cited below). Second, the initial characterization of returned martian samples contained within a sample-receiving facility (Chapters 6 and 7), which will be used to guide subsampling for biohazard testing and to inform decisions about sample allocations for further testing, or release from containment, will require understanding of the nature and origin of any organic matter present, whether derived from inorganic sources, from living or dormant life forms, or from fossils. For these reasons, it is prudent to briefly review some of the studies of biosignature capture and preservation that have been carried out in relevant terrestrial environments over the past decade. The number of published studies is substantial, and only a brief review of examples is provided here. 

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 ASSESSMENT OF PLANETARY PROTECTION REQUIREMENTS FOR MARS SAMPLE RETURN MISSIONS There have been numerous biosignature studies of terrestrial environments that have been considered analogs for Mars, particularly early in the planet’s history. Such studies have helped refine strategies for the astrobiological exploration of Mars, while defining new approaches for life detection. Studies of hydrothermal springs over a broad range of pH and mineralogy (including siliceous,4,5,6 travertine,7,8 and iron oxide-precipitating systems,9,10) have shown that biosignatures of thermophiles are commonly captured and preserved in both surface and subsurface hydrothermal deposits.11 In addition, a variety of studies have revealed good organic preservation in deposits of low-temperature surface springs and streams, over a broad range of pH from acidic12,13,14 to alkaline.15,16 Studies of modern and ancient evaporite deposits have also shown that microor- ganisms and their remains are commonly entrapped in a variety of salts, particularly sulfates and halides, both as solid inclusions and within fluid inclusions (Figure 4.1; see also Figure 6.2). 17,18,19,20,21,22 In addition, studies of sedimentary rocks that have experienced significant diagenesis, or alteration under low- to medium-grade meta- morphism, also retain fossil organic materials (e.g., kerogen).23 Microbial biosignatures are not restricted to surface deposits but have also been described from mineralized subsurface fractures and other void spaces in subsurface volcanic rocks.24,25 Finally, glacial ice and permafrost have been shown to harbor a broad range of extant and dormant life forms, as well as their cryopreserved fossil remains within water and brine-filled voids. 26,27 The recent discovery of sulfate-rich evaporite deposits by the Opportunity rover (see Figure 2.2) and both Mars Express and the Mars Reconnaissance Orbiter have elevated scientific interest in evaporite deposits as potential targets for a martian fossil record (Chapter 2). Similarly, recent orbital detections of phyllosilicates at many loca- tions on Mars28 have stimulated interest in Mars-analog studies of clay-rich sedimentary systems, which on Earth often provide favorable conditions for the preservation of organic materials. 29,30 Hydrated forms of silica have been shown to precipitate in a variety of aqueous settings, ranging from hydrothermal springs to low-temperature weathering environments. In terrestrial hot springs, silica has been shown to be a particularly favorable medium for preserving organic remains.31 Recent detections of amorphous hydrated silica (opal) by the Spirit rover32 and FIGURE 4.1 Microorganisms in fluid inclusions in evaporate crystals. A—Several microbes in fluid inclusions in 31,000-year- 4.1_from word.eps old halite from 16.7-meter depth in a core from Death Valley. Scale bar = 2 μm. SOURCE: Image courtesy of Brian Schubert, bitmap image Binghamton University. B—Yellow algae in a fluid inclusion in modern halite from an acid saline lake in Western Australia. Scale bar = 10 μm. SOURCE: Photograph courtesy of Tim Lowenstein and Michael Timofeeff, Binghamton University. C—Suspect microorganisms (one in focus and one out of focus) in a fluid inclusion in modern gypsum from an acid saline lake in Western Australia. Scale bar = 2 μm. SOURCE: Courtesy of Kathleen Benison, Central Michigan University.

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 THE POTENTIAL FOR FINDING BIOSIGNATURES IN RETURNED MARTIAN SAMPLES the Mars Reconnaissance Orbiter33,34 have underscored the need to better understand the range of conditions under which silica deposits form and the potential that silica-rich deposits have to capture and preserve biosignatures. Hydrothermal springs, seeps, and fumaroles have also been identified as important analogs for Special Regions on Mars.35 On Earth, hydrothermal springs support highly productive microbial ecosystems that often coexist with high rates of mineral precipitation.36 This situation favors the entombment of numerous microorganisms and their bioproducts as microfossils, as distinctive biologically mediated microfabrics, and as mesoscale biosedimentary structures, called microbialites.37 The long-term viability of microorganisms entombed in such deposits is an inter- esting area for future research. In addition, circulating crustal fluids have the potential to entrain deep-subsurface organisms and deliver them to surface environments where they may be captured and preserved in a viable state within associated mineral deposits and/or ground ice or permafrost (Figure 4.2). 38 Equally interesting from the standpoint of Special Regions are recently discovered evaporite deposits on Mars,39,40 including possible halite salts, which are the current record holders on Earth for the prolonged preser- vation of entombed, viable microorganisms.41,42 Finally, biosignature studies of martian analog environments and materials on Earth have also stimulated the development of new instrument and payload concepts to support future life detection missions on Mars.43,44,45 FIGURE 4.2 Photomicrograph of a thin section of a siliceous hot spring (sinter) deposit from the Midway Geyser Basin, 4.2_from word.eps Yellowstone National Park, Wyoming, showing heterogeneous microscale fabrics and the fossilized remains of filamentous bacteria. The image is approximately 0.63bitmap image (heavily sliced) mm across. SOURCE: Photograph courtesy of Jack D. Farmer, Arizona State University.

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0 ASSESSMENT OF PLANETARY PROTECTION REQUIREMENTS FOR MARS SAMPLE RETURN MISSIONS FIGURE 4.3 Photomicrograph showing a petrographic thin-section view of a finely laminated, carbonaceous shale from the Proterozoic Kajrahat Black Shale of the Vindhyan Supergroup, India. Dark laminae are enriched in organic carbon of microbial origin. SOURCE: Image courtesy of Jürgen Schieber, Indiana University; see http://www.shale-mudstone-research-schieber. indiana.edu/. This image was published in J. Schieber, S. Sur, and S. Banerjee, “Benthic Microbial Mats in Black Shale Units from the Vindhyan Supergroup, Middle Proterozoic of India: The Challenges of Recognizing the Genuine Article,” pp. 189- 197 in Atlas of Microbial Mat Features Preserved Within the Siliciclastic Rock Record (J. Schieber, P.K. Bose, P.G. Eriksson, S. Banerjee, S. Sarkar, W. Altermann, and O. Catuneanu, eds.), Copyright Elsevier, 2007. Many of the same challenges faced in the search for fossil biosignatures in ancient rocks on Earth are directly relevant to the exploration for a fossil record on Mars.46 Debates over the interpretation of biosignatures preserved in the earliest Precambrian fossil records on Earth47,48,49,50,51,52,53,54 and putative biosignatures in martian mete- orite ALH 8400155 have stimulated new approaches to fossil biosignature analysis56,57,58 and directly influenced approaches to Mars exploration.59 Investigations of Earth’s ancient geological record have also provided access to a geological record of ancient environments that were likely similar to early, potentially habitable, martian environments. It is generally assumed that life may have existed on Earth for more than 3.8 billion years. 60, 61,62 However, proving a biological origin for physical and chemical features found in ancient rocks is often challenged by poor preservation, or confusion arising from morphological and/or chemical convergence between biological and non- biological features and processes (Figure 4.3). This is well illustrated by the persistence of debates over putative signs of life in martian meteorite ALH 84001.63 The identification of definitive fossil biosignatures in martian samples could prove equally controversial, thus justifying the importance of Mars sample return. It is important to point out that biosignature research is a field that is still in its infancy. Although the pursuit of multiple lines of evidence consistent with biology may be a sufficient approach to biosignature analysis on a planet where life is both widespread and abundant, this strategy could prove insufficient for resolving questions of biogenicity with materials of extraterrestrial origin, as is well illustrated by the controversy over biosignatures in ALH 84001.

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 THE POTENTIAL FOR FINDING BIOSIGNATURES IN RETURNED MARTIAN SAMPLES CONCLuSIONS Geobiological studies of both modern and ancient Mars-relevant environments on Earth have highlighted the potential for samples returned from Mars to contain viable microorganisms or their fossilized remains, while supporting the development of new approaches for in situ and laboratory detections of biosignatures in a variety of geological materials. The committee found that uncertainties in the current assessment of martian habitability and of the potential for the inclusion of living entities in samples returned from Mars might be reduced by continuing research and development in the following areas: • Investigations of the prolonged viability of microorganisms in geological materials; • Studies of the nature and potential for biosignature preservation in a wide range of Mars-analog materials; • Evaluation of the impacts of post-depositional (diagenetic) processes (deep burial, impact shock, subfreez- ing temperatures) on the long-term retention of biosignatures in ancient geological materials; • Definition of reliable criteria for the definitive identification of biosignatures in ancient materials; and • Development of new laboratory-based and in situ analytical approaches to biosignature analysis. NOTES 1 . J.D. Farmer and D.J. Des Marais, “Exploring for a Record of Ancient Martian Life,” Journal of Geophysical Research—Planets 104(E11):26977-26995, 1999. 2 . B.A. Hofmann, J.D. Farmer, F. Von Blanckenburg, and A.E. Fallick, “Subsurface Filamentous Fabrics: An Evaluation of Origins Based on Morphological and Geochemical Criteria, with Implications for Exopaleontology,” Astrobiology 8:87-117, 2008. 3 . J.D. Farmer, “Exploring for a Fossil Record of Extraterrestrial Life,” pp. 10-15 in Palaeobiology II (D. Briggs and P. Crowther, eds.), Blackwell Science Publishers, Oxford, U.K., 2000. 4 . S.L. Cady and J.D. Farmer, “Fossilization Processes in Siliceous Thermal Springs: Trends in Preservation Along Thermal Gradients,” pp. 150-173 in Evolution of Hydrothermal Ecosystems on Earth (G.R. Bock and J.A. Goode, eds.), John Wiley and Sons Ltd., Chichester, U.K., 1996. 5 . R.W. Renaut and B. Jones, “Microbial Precipitates Around Continental Hot Springs and Geysers,” pp. 187-195 in Microbial Sediments (R. Riding and S. Awramik, eds.), Springer, Berlin, 2000. 6 . K.M. Handley, S.J. Turner, K.A. Campbell, and B.W. Mountain, “Silicifying Biofilm Exopolymers on a Hot-Spring Microstromatolite: Templating Nanometer-Thick Laminae,” Astrobiology 8:747-770, 2008. 7 . B.W. Fouke, G.T. Bonheyo, B. Sanzenbacher, and J. Frias-Lopez, “Partitioning of Bacterial Communities Between Travertine Depositional Facies at Mammoth Hot Springs, Yellowstone National Park, U.S.A.,” Canadian Journal of Earth Sciences 40:1531-1548, 2003. 8 . A. Pentecost, “Cyanobacteria Associated with Hot Spring Travertines,” Canadian Journal of Earth Sciences 40:1447- 1457, 2003. 9 . B.K. Pierson and M.T. Parenteau, “Phototrophs in High Iron Microbial Mats: Microstructure of Mats in Iron- depositing Hot Springs,” FEMS Microbiology Ecology 32:181-196, 2000. 10 . M.L. Wade, D.G. Agresti, T.J. Wdowiak, L.P. Armendarez, and J.D. Farmer, “A Mössbauer Investigation of Iron- rich Terrestrial Hydrothermal Vent Systems: Lessons for Mars Exploration,” Journal of Geophysical Research—Planets 104(E4):8489-8507, 1999. 11 . B.A. Hofmann, J.D. Farmer, F. von Blanckenburg, and A.E. Fallick, “Subsurface Filamentous Fabrics: An Evaluation of Origins Based on Morphological and Geochemical Criteria, with Implications for Exopaleontology,” Astrobiology 8:87-117, 2008. 12 . D.C. Fernandez-Remolar and A.H. Knoll, “Fossilization Potential of Iron-bearing Minerals in Acidic Environments of Rio Tinto, Spain: Implications for Mars Exploration,” Icarus, 194:72-85, 2008. 13 . K.C. Benison and B.B. Bowen, “Acid Saline Lake Systems Give Clues About Past Environments and the Search for Life on Mars,” Icarus 183:225-229, 2006. 14 . K.C. Benison, “A Martian Analog in Kansas: Comparing Martian Strata with Permian Acid Saline Lake Deposits,” Geology 34:385-388, 2006.

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