Unraveling biogeochemical phosphorus dynamics in hyperarid Mars-analogue soils using stable oxygen isotopes in phosphate
Corresponding Author
Jianxun Shen
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, UK
Correspondence
Jianxun Shen, School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews KY16 9AL, UK.
Email: js365@st-andrews.ac.uk
Search for more papers by this authorAndrew C. Smith
NERC Isotope Geosciences Facilities, British Geological Survey, Nottingham, UK
Search for more papers by this authorMark W. Claire
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, UK
Search for more papers by this authorAubrey L. Zerkle
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, UK
Search for more papers by this authorCorresponding Author
Jianxun Shen
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, UK
Correspondence
Jianxun Shen, School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews KY16 9AL, UK.
Email: js365@st-andrews.ac.uk
Search for more papers by this authorAndrew C. Smith
NERC Isotope Geosciences Facilities, British Geological Survey, Nottingham, UK
Search for more papers by this authorMark W. Claire
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, UK
Search for more papers by this authorAubrey L. Zerkle
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews, UK
Search for more papers by this authorFunding Information
This project has received funding from the European Research Council under the European Union’s Horizon 2020 Research and Innovation Programme (Grant 678812 to M.W.C.). J.S. also acknowledges support from the China Scholarship Council (CSC).
Abstract
With annual precipitation less than 20 mm and extreme UV intensity, the Atacama Desert in northern Chile has long been utilized as an analogue for recent Mars. In these hyperarid environments, water and biomass are extremely limited, and thus, it becomes difficult to generate a full picture of biogeochemical phosphate-water dynamics. To address this problem, we sampled soils from five Atacama study sites and conducted three main analyses—stable oxygen isotopes in phosphate, enzyme pathway predictions, and cell culture experiments. We found that high sedimentation rates decrease the relative size of the organic phosphorus pool, which appears to hinder extremophiles. Phosphoenzyme and pathway prediction analyses imply that inorganic pyrophosphatase is the most likely catalytic agent to cycle P in these environments, and this process will rapidly overtake other P utilization strategies. In these soils, the biogenic δ18O signatures of the soil phosphate (δ18OPO4) can slowly overprint lithogenic δ18OPO4 values over a timescale of tens to hundreds of millions of years when annual precipitation is more than 10 mm. The δ18OPO4 of calcium-bound phosphate minerals seems to preserve the δ18O signature of the water used for biogeochemical P cycling, pointing toward sporadic rainfall and gypsum hydration water as key moisture sources. Where precipitation is less than 2 mm, biological cycling is restricted and bedrock δ18OPO4 values are preserved. This study demonstrates the utility of δ18OPO4 values as indicative of biogeochemical cycling and hydrodynamics in an extremely dry Mars-analogue environment.
Conflict of Interest
We have no conflict of interest to declare.
Open Research
Data Availability Statement
Sequencing data for enzyme and pathway analyses in this study can be found in the National Center for Biotechnology Information (NCBI) under the Sequence Read Archive (SRA) accession numbers of SRX7370993, SRX7370998, and SRX7370989.
References
- Adcock, C. T., Hausrath, E. M., & Forster, P. M. (2013). Readily available phosphate from minerals in early aqueous environments on Mars. Nature Geoscience, 6(10), 824–827. https://doi.org/10.1038/Ngeo1923.
- Alpers, C. N., & Whittemore, D. O. (1990). Hydrogeochemistry and Stable Isotopes of Ground and Surface Waters from 2 Adjacent Closed Basins, Atacama Desert. Northern Chile. Applied Geochemistry, 5(5–6), 719–734. https://doi.org/10.1016/0883-2927(90)90067-F.
- Altheide, T., Chevrier, V., Nicholson, C., & Denson, J. (2009). Experimental investigation of the stability and evaporation of sulfate and chloride brines on Mars. Earth and Planetary Science Letters, 282(1–4), 69–78. https://doi.org/10.1016/j.epsl.2009.03.002.
- Ameen, F., AlYahya, S. A., AlNadhari, S., Alasmari, H., Alhoshani, F., & Wainwright, M. (2019). Phosphate solubilizing bacteria and fungi in desert soils: species, limitations and mechanisms. Archives of Agronomy and Soil Science, 65(10), 1446–1459. https://doi.org/10.1080/03650340.2019.1566713.
- Amelung, W., Blume, H.-P., Fleige, H., Horn, R., Kandeler, E., Kögel-Knabner, I., … Wilke, B.-M. (2018). Scheffer/Schachtschabel Lehrbuch der Bodenkunde. Heidelberg, Berlin: Springer-Verlag.
10.1007/978-3-662-55871-3 Google Scholar
- Angert, A., Weiner, T., Mazeh, S., & Sternberg, M. (2012). Soil Phosphate Stable Oxygen Isotopes across Rainfall and Bedrock Gradients. Environmental Science & Technology, 46(4), 2156–2162. https://doi.org/10.1021/es203551s.
- Aravena, R., Peña, H., Grilli, A., Suzuki, O., & Mordeckai, M. (1989). Evolución isotópica de las lluvias y origen de las masas de aire en el Altiplano chileno (pp. 129–142). Vienna: Isotope Hydrology Investigations in Latin America. IAEA.
- Aravena, R., Suzuki, O., Pena, H., Pollastri, A., Fuenzalida, H., & Grilli, A. (1999). Isotopic composition and origin of the precipitation in Northern Chile. Applied Geochemistry, 14(4), 411–422. https://doi.org/10.1016/S0883-2927(98)00067-5.
- Aravena, R., Suzuki, O., & Pollastri, A. (1989). Coastal Fog and Its Relation to Groundwater in the Iv-Region of Northern Chile. Chemical Geology, 79(1), 83–91. https://doi.org/10.1016/0168-9622(89)90008-0.
- Azua-Bustos, A., Caro-Lara, L., & Vicuna, R. (2015). Discovery and microbial content of the driest site of the hyperarid Atacama Desert. Chile. Environmental Microbiology Reports, 7(3), 388–394. https://doi.org/10.1111/1758-2229.12261.
- Azua-Bustos, A., Fairen, A. G., Gonzalez-Silva, C., Ascaso, C., Carrizo, D., Fernandez-Martinez, M. A., … Parro, V. (2018). Unprecedented rains decimate surface microbial communities in the hyperarid core of the Atacama Desert. Scientific Reports, 8, 16706. https://doi.org/10.1038/s41598-018-35051-w.
- Azua-Bustos, A., Gonzalez-Silva, C., Mancilla, R. A., Salas, L., Gomez-Silva, B., McKay, C. P., & Vicuna, R. (2011). Hypolithic Cyanobacteria Supported Mainly by Fog in the Coastal Range of the Atacama Desert. Microbial Ecology, 61(3), 568–581. https://doi.org/10.1007/s00248-010-9784-5.
- Bagaley, D. R. (2006). Uncovering bacterial diversity on and below the surface of a hyper-arid environment, the Atacama Desert, Chile. (Master of Science), Louisiana State University and Agricultural and Mechanical College.
- Barbera, P., Kozlov, A. M., Czech, L., Morel, B., Darriba, D., Flouri, T., & Stamatakis, A. (2019). EPA-ng: Massively Parallel Evolutionary Placement of Genetic Sequences. Systematic Biology, 68(2), 365–369. https://doi.org/10.1093/sysbio/syy054.
- Barker, D. S. (1978). Magmatic Trends on Alkali-Iron-Magnesium Diagrams. American Mineralogist, 63(5–6), 531–534.
- Blake, R. E. (1998). Enzyme-catalyzed oxygen isotope exchange between inorganic phosphate and water: Reaction rates and temperature dependence at 5.7-30℃. Mineralogical Magazine, 62, 163–164.
10.1180/minmag.1998.62A.1.87 Google Scholar
- Blake, R. E., Alt, J. C., & Martini, A. M. (2001). Oxygen isotope ratios of PO4: An inorganic indicator of enzymatic activity and P metabolism and a new biomarker in the search for life. Proceedings of the National Academy of Sciences of the United States of America, 98(5), 2148–2153. https://doi.org/10.1073/pnas.051515898.
- Blake, R. E., Chang, S. J., & Lepland, A. (2010). Phosphate oxygen isotopic evidence for a temperate and biologically active Archaean ocean. Nature, 464(7291), 113–145. https://doi.org/10.1038/nature08952.
- Blake, R. E., O'Neil, J. R., & Surkov, A. V. (2005). Biogeochemical cycling of phosphorus: Insights from oxygen isotope effects of phosphoenzymes. American Journal of Science, 305(6–8), 596–620. https://doi.org/10.2475/ajs.305.6-8.596.
- Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., … Caporaso, J. G. (2019). Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology, 37(8), 852–857. https://doi.org/10.1038/s41587-019-0209-9.
- Boschetti, T., Cifuentes, J., Iacumin, P., & Selmo, E. (2019). Local Meteoric Water Line of Northern Chile (18 degrees S-30 degrees S): An Application of Error-in-Variables Regression to the Oxygen and Hydrogen Stable Isotope Ratio of Precipitation. Water, 11(4), 791. https://doi.org/10.3390/w11040791.
- Broadhurst, F. M., & Loring, D. H. (1970). Rates of Sedimentation in Upper Carboniferous of Britain. Lethaia, 3(1), 1. https://doi.org/10.1111/j.1502-3931.1970.tb01260.x.
- Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13(7), 581. https://doi.org/10.1038/Nmeth.3869.
- Cappa, C. D., Hendricks, M. B., DePaolo, D. J., & Cohen, R. C. (2003). Isotopic fractionation of water during evaporation. Journal of Geophysical Research-Atmospheres, 108(D16), 4525. https://doi.org/10.1029/2003jd003597.
- Caspi, R., Billington, R., Ferrer, L., Foerster, H., Fulcher, C. A., Keseler, I. M., … Karp, P. D. (2016). The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Research, 44(D1), D471–480. https://doi.org/10.1093/nar/gkv1164.
- Caspi, R., Billington, R., Fulcher, C. A., Keseler, I. M., Kothari, A., Krummenacker, M., … Karp, P. D. (2018). The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Research, 46(D1), D633–D639. https://doi.org/10.1093/nar/gkx935.
- Chang, S. J., & Blake, R. E. (2015). Precise calibration of equilibrium oxygen isotope fractionations between dissolved phosphate and water from 3 to 37 degrees C. Geochimica Et Cosmochimica Acta, 150, 314–329. https://doi.org/10.1016/j.gca.2014.10.030.
- Chevrier, V., Hanley, J., & Altheide, T. (2009). Stability of perchlorate hydrates and their liquid solutions at the Phoenix landing site, Mars (vol 36, art no L10202, 2009). Geophysical Research Letters, 36, 14. https://doi.org/10.1029/2009gl040523.
- Chislock, M. F., Doster, E., Zitomer, R. A., & Wilson, A. (2013). Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nature Education Knowledge, 4(4), 10.
- Cho, H. S., Seo, S. W., Kim, Y. M., Jung, G. Y., & Park, J. M. (2012). Engineering glyceraldehyde-3-phosphate dehydrogenase for switching control of glycolysis in Escherichia coli. Biotechnology and Bioengineering, 109(10), 2612–2619. https://doi.org/10.1002/bit.24532.
- Cleveland, C. C., & Liptzin, D. (2007). C : N : P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochemistry, 85(3), 235–252. https://doi.org/10.1007/s10533-007-9132-0.
- Clifford, S. M., & Parker, T. J. (2001). The evolution of the Martian hydrosphere: Implications for the fate of a primordial ocean and the current state of the northern plains. Icarus, 154(1), 40–79. https://doi.org/10.1006/icar.2001.6671.
- Coleman, N. M., Dinwiddie, C. L., & Casteel, K. (2007). High outflow channels on Mars indicate Hesperian recharge at low latitudes and the presence of Canyon Lakes. Icarus, 189(2), 344–361. https://doi.org/10.1016/j.icarus.2007.01.020.
- Cordero, R. R., Damiani, A., Jorquera, J., Sepulveda, E., Caballero, M., Fernandez, S., … Labbe, F. (2018). Ultraviolet radiation in the Atacama Desert. Antonie Van Leeuwenhoek, 111(8), 1301–1313. https://doi.org/10.1007/s10482-018-1075-z.
- Craddock, R. A., & Howard, A. D. (2002). The case for rainfall on a warm, wet early Mars. Journal of Geophysical Research-Planets, 107(E11), 1505. https://doi.org/10.1029/2001je001505.
- Crain, G. M., McLaren, J. R., Brunner, B., & Darrouzet-Nardi, A. (2018). Biologically Available Phosphorus in Biocrust-Dominated Soils of the Chihuahuan Desert. Soil Systems, 2(4), 56. https://doi.org/10.3390/soilsystems2040056.
- Crits-Christoph, A., Robinson, C. K., Barnum, T., Fricke, W. F., Davila, A. F., Jedynak, B., … DiRuggiero, J. (2013). Colonization patterns of soil microbial communities in the Atacama Desert. Microbiome, 1, 28. https://doi.org/10.1186/2049-2618-1-28.
- Cull, S. C., Arvidson, R. E., Catalano, J. G., Ming, D. W., Morris, R. V., Mellon, M. T., & Lemmon, M. (2010). Concentrated perchlorate at the Mars Phoenix landing site: Evidence for thin film liquid water on Mars. Geophysical Research Letters, 37, 22. https://doi.org/10.1029/2010gl045269.
- Czech, L., & Stamatakis, A. (2019). Scalable methods for analyzing and visualizing phylogenetic placement of metagenomic samples. Plos One, 14(5), e0217050. https://doi.org/10.1371/journal.pone.0217050.
- Dahms, A. S., & Boyer, P. D. (1973). Occurrence and Characteristics of O-18 Exchange-Reactions Catalyzed by Sodium-Dependent and Potassium-Dependent Adenosine Triphosphatases. Journal of Biological Chemistry, 248(9), 3155–3162.
- Dansgaard, W. (1964). Stable Isotopes in Precipitation. Tellus, 16(4), 436–468.
- Di Achille, G., & Hynek, B. M. (2010). Ancient ocean on Mars supported by global distribution of deltas and valleys. Nature Geoscience, 3(7), 459–463. https://doi.org/10.1038/Ngeo891.
- Di Achille, G., Ori, G. G., & Reiss, D. (2007). Evidence for late Hesperian lacustrine activity in Shalbatana Vallis, Mars. Journal of Geophysical Research-Planets, 112(E7), e002858. https://doi.org/10.1029/2006je002858.
- Dong, H. L., Rech, J. A., Jiang, H. C., Sun, H., & Buck, B. J. (2007). Endolithic cyanobacteria in soil gypsum: Occurrences in Atacama (Chile), Mojave (United States), and Al-Jafr Basin (Jordan) deserts. Journal of Geophysical Research-Biogeosciences, 112(G2), G02030. https://doi.org/10.1029/2006jg000385.
- Douglas, G. M., Maffei, V. J., Zaneveld, J., Yurgel, S. N., Brown, J. R., Taylor, C. M., …Langille, M. G. (2019). PICRUSt2: An improved and extensible approach for metagenome inference. BioRxiv, 672295.
- Dunai, T. J., Lopez, G. A. G., & Juez-Larre, J. (2005). Oligocene-Miocene age of aridity in the Atacama Desert revealed by exposure dating of erosion-sensitive landforms. Geology, 33(4), 321–324. https://doi.org/10.1130/G21184.1.
- Eddy, S., & Wheeler, T. (2007). HMMER-biosequence analysis using profile hidden Markov models. Retrieved from http://hmmer.janelia.org.
- Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16), 2194–2200. https://doi.org/10.1093/bioinformatics/btr381.
- Ewing, S. A., Michalski, G., Thiemens, M., Quinn, R. C., Macalady, J. L., Kohl, S., … Amundson, R. (2007). Rainfall limit of the N cycle on Earth. Global Biogeochemical Cycles, 21, 3. https://doi.org/10.1029/2006gb002838.
- Fabre, A., Gauquelin, T., Vilasante, F., Ortega, A., & Puig, H. (2006). Phosphorus content in five representative landscape units of the Lomas de Arequipa (Atacama Desert-Peru). Catena, 65(1), 80–86. https://doi.org/10.1016/j.catena.2005.10.004.
- Farias, M. E., Contreras, M., Rasuk, M. C., Kurth, D., Flores, M. R., Poire, D. G., … Visscher, P. T. (2014). Characterization of bacterial diversity associated with microbial mats, gypsum evaporites and carbonate microbialites in thalassic wetlands: Tebenquiche and La Brava, Salar de Atacama, Chile. Extremophiles, 18(2), 311–329. https://doi.org/10.1007/s00792-013-0617-6.
- Farmer, G. (2003). Continental basaltic rocks. Treatise on Geochemistry, 3, 659.
- Fritz, P., Suzuki, O., Silva, C., & Salati, E. (1981). Isotope Hydrology of Groundwaters in the Pampa Del Tamarugal. Chile. Journal of Hydrology, 53(1–2), 161–184. https://doi.org/10.1016/0022-1694(81)90043-3.
- Garreaud, R. D., Molina, A., & Farias, M. (2010). Andean uplift, ocean cooling and Atacama hyperaridity: A climate modeling perspective. Earth and Planetary Science Letters, 292(1–2), 39–50. https://doi.org/10.1016/j.epsl.2010.01.017.
- Garreaud, R. D., Vuille, M., Compagnucci, R., & Marengo, J. (2009). Present-day South American climate. Palaeogeography Palaeoclimatology Palaeoecology, 281(3–4), 180–195. https://doi.org/10.1016/j.palaeo.2007.10.032.
- Gazquez, F., Evans, N. P., & Hodell, D. A. (2017). Precise and accurate isotope fractionation factors (alpha O-17, alpha O-18 and alpha D) for water and CaSO4 center dot 2H(2)O (gypsum). Geochimica Et Cosmochimica Acta, 198, 259–270. https://doi.org/10.1016/j.gca.2016.11.001.
- George, T. S., Giles, C. D., Menezes-Blackburn, D., Condron, L. M., Gama-Rodrigues, A. C., Jaisi, D., … Haygarth, P. M. (2018). Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities (vol 427, pg 191, 2018). Plant and Soil, 427(1–2), 209–211. https://doi.org/10.1007/s11104-017-3488-2.
- Golterman, H. L. (1973). Natural Phosphate Sources in Relation to Phosphate Budgets - Contribution to Understanding of Eutrophication. Water Research, 7(1–2), 3–17. https://doi.org/10.1016/0043-1354(73)90149-8.
- Granger, S. J., Yang, Y. G., Pfahler, V., Hodgson, C., Smith, A. C., Le Cocq, K., … Howden, N. J. K. (2018). The stable oxygen isotope ratio of resin extractable phosphate derived from fresh cattle faeces. Rapid Communications in Mass Spectrometry, 32(9), 703–710. https://doi.org/10.1002/rcm.8092.
- Gross, A., & Angert, A. (2015). What processes control the oxygen isotopes of soil bio-available phosphate? Geochimica Et Cosmochimica Acta, 159, 100–111. https://doi.org/10.1016/j.gca.2015.03.023.
- Gross, A., Turner, B. L., Wright, S. J., Tanner, E. V. J., Reichstein, M., Weiner, T., & Angert, A. (2015). Oxygen isotope ratios of plant available phosphate in lowland tropical forest soils. Soil Biology & Biochemistry, 88, 354–361. https://doi.org/10.1016/j.soilbio.2015.06.015.
- Guidry, M. W., & Mackenzie, F. T. (2003). Experimental study of igneous and sedimentary apatite dissolution: control of pH, distance from equilibrium, and temperature on dissolution rates. Geochimica Et Cosmochimica Acta, 67(16), 2949–2963. https://doi.org/10.1016/S0016-7037(03)00265-5.
- Gyaneshwar, P., Kumar, G. N., & Parekh, L. J. (1998). Effect of buffering on the phosphate-solubilizing ability of microorganisms. World Journal of Microbiology & Biotechnology, 14(5), 669–673. https://doi.org/10.1023/A:1008852718733.
- Hartley, A. J., Chong, G., Houston, J., & Mather, A. E. (2005). 150 million years of climatic stability: evidence from the Atacama Desert, northern Chile. Journal of the Geological Society, 162, 421–424. https://doi.org/10.1144/0016-764904-071.
- Hecht, M. H., Kounaves, S. P., Quinn, R. C., West, S. J., Young, S. M. M., Ming, D. W., … Smith, P. H. (2009). Detection of Perchlorate and the Soluble Chemistry of Martian Soil at the Phoenix Lander Site. Science, 325(5936), 64–67. https://doi.org/10.1126/science.1172466.
- Hedley, M. J., Stewart, J. W. B., & Chauhan, B. S. (1982). Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Science Society of America Journal, 46(5), 970–976. https://doi.org/10.2136/sssaj1982.03615995004600050017x.
- Helfenstein, J., Pistocchi, C., Oberson, A., Tamburini, F., Goll, D. S., & Frossard, E. (2020). Estimates of mean residence times of phosphorus in commonly considered inorganic soil phosphorus pools. Biogeosciences, 17(2), 441–454. https://doi.org/10.3929/ethz-b-000399324.
- Helfenstein, J., Tamburini, F., von Sperber, C., Massey, M. S., Pistocchi, C., Chadwick, O. A., … Frossard, E. (2018). Combining spectroscopic and isotopic techniques gives a dynamic view of phosphorus cycling in soil. Nature Communications, 9, 3226. https://doi.org/10.1038/s41467-018-05731-2.
- Herlemann, D. P. R., Labrenz, M., Jurgens, K., Bertilsson, S., Waniek, J. J., & Andersson, A. F. (2011). Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. Isme Journal, 5(10), 1571–1579. https://doi.org/10.1038/ismej.2011.41.
- Herrera, C., Gamboa, C., Custodio, E., Jordan, T., Godfrey, L., Jodar, J., … Saez, A. (2018). Groundwater origin and recharge in the hyperarid Cordillera de la Costa, Atacama Desert, northern Chile. Science of the Total Environment, 624, 114–132. https://doi.org/10.1016/j.scitotenv.2017.12.134.
- Houston, J. (2006). Variability of precipitation in the Atacama desert: Its causes and hydrological impact. International Journal of Climatology, 26(15), 2181–2198. https://doi.org/10.1002/joc.1359.
- Houston, J., & Hartley, A. J. (2003). The central andean west-slope rainshadow and its potential contribution to the origin of HYPER-ARIDITY in the Atacama desert. International Journal of Climatology, 23(12), 1453–1464. https://doi.org/10.1002/joc.938.
- Hsieh, J. C. C., Chadwick, O. A., Kelly, E. F., & Savin, S. M. (1998). Oxygen isotopic composition of soil water: quantifying evaporation and transpiration. Geoderma, 82(1–3), 269–293. https://doi.org/10.1016/S0016-7061(97)00105-5.
- Huang, J. Y., Wang, P., Niu, Y. B., Yu, H. L., Ma, F., Xiao, G. J., & Xu, X. (2018). Changes in C:N: P stoichiometry modify N and P conservation strategies of a desert steppe species Glycyrrhiza uralensis. Scientific Reports, 8, 12668. https://doi.org/10.1038/s41598-018-30324-w.
- Hynek, B. M., Beach, M., & Hoke, M. R. T. (2010). Updated global map of Martian valley networks and implications for climate and hydrologic processes. Journal of Geophysical Research, 115, E09008. https://doi.org/10.1029/2009JE003548.
- Illmer, P., & Schinner, F. (1992). Solubilization of Inorganic Phosphates by Microorganisms Isolated from Forest Soils. Soil Biology & Biochemistry, 24(4), 389–395. https://doi.org/10.1016/0038-0717(92)90199-8.
- Irwin, R. P., Maxwell, T. A., Howard, A. D., Craddock, R. A., & Leverington, D. W. (2002). A large paleolake basin at the head of Ma'adim Vallis, Mars. Science, 296(5576), 2209–2212. https://doi.org/10.1126/science.1071143.
- Jaisi, D. P., & Blake, R. E. (2010). Tracing sources and cycling of phosphorus in Peru Margin sediments using oxygen isotopes in authigenic and detrital phosphates. Geochimica Et Cosmochimica Acta, 74(11), 3199–3212. https://doi.org/10.1016/j.gca.2010.02.030.
- Jaisi, D. P., & Blake, R. E. (2014). Advances in using oxygen isotope ratios of phosphate to understand phosphorus cycling in the environment. Advances in Agronomy, 125, 1–53.
- Jaisi, D. P., Blake, R. E., & Kukkadapu, R. K. (2010). Fractionation of oxygen isotopes in phosphate during its interactions with iron oxides. Geochimica Et Cosmochimica Acta, 74(4), 1309–1319. https://doi.org/10.1016/j.gca.2009.11.010.
- Jaisi, D. P., Kukkadapu, R. K., Stout, L. M., Varga, T., & Blake, R. E. (2011). Biotic and Abiotic Pathways of Phosphorus Cycling in Minerals and Sediments: Insights from Oxygen Isotope Ratios in Phosphate. Environmental Science & Technology, 45(15), 6254–6261. https://doi.org/10.1021/es200456e.
- Johnson, L. S., Eddy, S. R., & Portugaly, E. (2010). Hidden Markov model speed heuristic and iterative HMM search procedure. Bmc Bioinformatics, 11, 431. https://doi.org/10.1186/1471-2105-11-431.
- Jordan, T. E., Herrera, C., Godfrey, L. V., Colucci, S. J., Gamboa, C., Urrutia, J., … Paul, J. F. (2019). Isotopic characteristics and paleoclimate implications of the extreme precipitation event of March 2015 in northern Chile. Andean Geology, 46(1), 1–31. https://doi.org/10.5027/andgeoV46n1-3087.
- Kereszturi, A., & Rivera-Valentin, E. G. (2012). Locations of thin liquid water layers on present-day Mars. Icarus, 221(1), 289–295. https://doi.org/10.1016/j.icarus.2012.08.004.
- Kirkham, R., Chorlton, J., & Carriere, J. (1995). Generalized geology of the world; Generalized geological map of the world and linked databases. Geological Survey of Canada, 2915D.
- Klindworth, A., Pruesse, E., Schweer, T., Peplies, J., Quast, C., Horn, M., & Glockner, F. O. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Research, 41(1), e1. https://doi.org/10.1093/nar/gks808.
- Knowles, J. R. (1980). Enzyme-catalyzed phosphoryl transfer reactions. Annual Review of Biochemistry, 49, 877–919. https://doi.org/10.1146/annurev.bi.49.070180.004305.
- Kolodny, Y., Luz, B., & Navon, O. (1983). Oxygen Isotope Variations in Phosphate of Biogenic Apatites. 1. Fish Bone Apatite - Rechecking the Rules of the Game. Earth and Planetary Science Letters, 64(3), 398–404. https://doi.org/10.1016/0012-821x(83)90100-0.
- Komatsu, G., & Ori, G. G. (2000). Exobiological implications of potential sedimentary deposits on Mars. Planetary and Space Science, 48(11), 1043–1052. https://doi.org/10.1016/S0032-0633(00)00078-7.
- Kouno, K., Tuchiya, Y., & Ando, T. (1995). Measurement of Soil Microbial Biomass Phosphorus by an Anion-Exchange Membrane Method. Soil Biology & Biochemistry, 27(10), 1353–1357. https://doi.org/10.1016/0038-0717(95)00057-L.
- Kreuzeder, A. (2011). Modelling phosphorus flows in soils. Göttingen: Optimus-Verlag.
- Lester, E. D., Satomi, M., & Ponce, A. (2007). Microflora of extreme arid Atacama Desert soils. Soil Biology & Biochemistry, 39(2), 704–708. https://doi.org/10.1016/j.soilbio.2006.09.020.
- Liang, Y., & Blake, R. E. (2006). Oxygen isotope signature of P-i regeneration from organic compounds by phosphomonoesterases and photooxidation. Geochimica Et Cosmochimica Acta, 70(15), 3957–3969. https://doi.org/10.1016/j.gca.2006.04.036.
- Liang, Y., & Blake, R. E. (2009). Compound- and enzyme-specific phosphodiester hydrolysis mechanisms revealed by delta O-18 of dissolved inorganic phosphate: Implications for marine P cycling. Geochimica Et Cosmochimica Acta, 73(13), 3782–3794. https://doi.org/10.1016/j.gca.2009.01.038.
- Louca, S., & Doebeli, M. (2018). Efficient comparative phylogenetics on large trees. Bioinformatics, 34(6), 1053–1055. https://doi.org/10.1093/bioinformatics/btx701.
- Lucassen, E. C. H. E. T., Smolders, A. J. P., Lamers, L. P. M., & Roelofs, J. G. M. (2005). Water table fluctuations and groundwater supply are important in preventing phosphate-eutrophication in sulphate-rich fens: Consequences for wetland restoration. Plant and Soil, 269(1–2), 109–115. https://doi.org/10.1007/s11104-004-0554-3.
- Makhalanyane, T. P., Valverde, A., Gunnigle, E., Frossard, A., Ramond, J. B., & Cowan, D. A. (2015). Microbial ecology of hot desert edaphic systems. FEMS Microbiol Rev, 39(2), 203–221. https://doi.org/10.1093/femsre/fuu011.
- Malin, M. C., & Edgett, K. S. (2003). Evidence for persistent flow and aqueous sedimentation on early Mars. Science, 302(5652), 1931–1934. https://doi.org/10.1126/science.1090544.
- Markel, D., Kolodny, Y., Luz, B., & Nishri, A. (1994). Phosphorus cycling and phosphorus sources in Lake Kinneret: tracing by oxygen isotopes in phosphate. Israel Journal of Earth Sciences, 43(3–4), 165–178.
- Martinez, G. M., & Renno, N. O. (2013). Water and Brines on Mars: Current Evidence and Implications for MSL. Space Science Reviews, 175(1–4), 29–51. https://doi.org/10.1007/s11214-012-9956-3.
- McIsaac, G. F., David, M. B., Gertner, G. Z., & Goolsby, D. A. (2001). Eutrophication - Nitrate flux in the Mississippi river. Nature, 414(6860), 166–167. https://doi.org/10.1038/35102672.
- McKay, C. P., Friedmann, E. I., Gomez-Silva, B., Caceres-Villanueva, L., Andersen, D. T., & Landheim, R. (2003). Temperature and moisture conditions for life in the extreme arid region of the Atacama Desert: Four years of observations including the El Nino of 1997–1998. Astrobiology, 3(2), 393–406. https://doi.org/10.1089/153110703769016460.
- Mclaughlin, M. J., Alston, A. M., & Martin, J. K. (1986). Measurement of Phosphorus in the Soil Microbial Biomass - a Modified Procedure for Field Soils. Soil Biology & Biochemistry, 18(4), 437–443. https://doi.org/10.1016/0038-0717(86)90050-7.
- Meng, J., Yao, Q. Z., & Yu, Z. G. (2014). Particulate phosphorus speciation and phosphate adsorption characteristics associated with sediment grain size. Ecological Engineering, 70, 140–145. https://doi.org/10.1016/j.ecoleng.2014.05.007.
- Meslin, P. Y., Gasnault, O., Forni, O., Schroder, S., Cousin, A., Berger, G., … Team, M. S. (2013). Soil Diversity and Hydration as Observed by ChemCam at Gale Crater, Mars. Science, 341(6153), 1238670. https://doi.org/10.1126/science.1238670.
- Michalski, G., Bohlke, J. K., & Thiemens, M. (2004). Long term atmospheric deposition as the source of nitrate and other salts in the Atacama Desert, Chile: New evidence from mass-independent oxygen isotopic compositions. Geochimica Et Cosmochimica Acta, 68(20), 4023–4038. https://doi.org/10.1016/j.gca.2004.04.009.
- Mizota, C., Domon, Y., & Yoshida, N. (1992). Oxygen Isotope Composition of Natural Phosphates from Volcanic Ash Soils of the Great Rift-Valley of Africa and East Java, Indonesia. Geoderma, 53(1–2), 111–123. https://doi.org/10.1016/0016-7061(92)90025-3.
- Mooney, H. A., Gulmon, S. L., Ehleringer, J., & Rundel, P. W. (1980). Atmospheric Water-Uptake by an Atacama Desert Shrub. Science, 209(4457), 693–694. https://doi.org/10.1126/science.209.4457.693.
- Murphy, J., & Riley, J. P. (1962). A Modified Single Solution Method for Determination of Phosphate in Natural Waters. Analytica Chimica Acta, 26(1), 31.
- Nahas, E. (1996). Factors determining rock phosphate solubilization by microorganisms isolated from soil. World Journal of Microbiology & Biotechnology, 12(6), 567–572. https://doi.org/10.1007/Bf00327716.
- Navarro-Gonzalez, R., Rainey, F. A., Molina, P., Bagaley, D. R., Hollen, B. J., de la Rosa, J., … McKay, C. P. (2003). Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science, 302(5647), 1018–1021. https://doi.org/10.1126/science.1089143.
- Oberlin, E. A., Claire, M. W., & Kounaves, S. P. (2018). Evaluation of the Tindouf Basin Region in Southern Morocco as an Analog Site for Soil Geochemistry on Noachian Mars. Astrobiology, 18(10), 1318–1328. https://doi.org/10.1089/ast.2016.1557.
- Oburger, E., Jones, D. L., & Wenzel, W. W. (2011). Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil. Plant and Soil, 341(1–2), 363–382. https://doi.org/10.1007/s11104-010-0650-5.
- Olivares, D., Ferrada, P., de Matos, C., Marzo, A., Cabrera, E., Portillo, C., & Llanos, J. (2017). Characterization of soiling on PV modules in the Atacama Desert. Energy Procedia, 124, 547–553. https://doi.org/10.1016/j.egypro.2017.09.263.
10.1016/j.egypro.2017.09.263 Google Scholar
- Olsen, S. R. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Department of Agriculture Circular, 939, 1–19.
- Orlando, J., Alfaro, M., Bravo, L., Guevara, R., & Caru, M. (2010). Bacterial diversity and occurrence of ammonia-oxidizing bacteria in the Atacama Desert soil during a "desert bloom" event. Soil Biology & Biochemistry, 42(7), 1183–1188. https://doi.org/10.1016/j.soilbio.2010.03.025.
- Osorio, N. W., & Habte, M. (2013). Phosphate desorption from the surface of soil mineral particles by a phosphate-solubilizing fungus. Biology and Fertility of Soils, 49(4), 481–486. https://doi.org/10.1007/s00374-012-0763-5.
- Palacio, S., Azorin, J., Montserrat-Marti, G., & Ferrio, J. P. (2014). The crystallization water of gypsum rocks is a relevant water source for plants. Nature Communications, 5, 4660. https://doi.org/10.1038/ncomms5660.
- Passariello, C., Forleo, C., Micheli, V., Schippa, S., Leone, R., Mangani, S., … Rossolini, G. M. (2006). Biochemical characterization of the class B acid phosphatase (AphA) of Escherichia coli MG1655. Biochimica Et Biophysica Acta-Proteins and Proteomics, 1764(1), 13–19. https://doi.org/10.1016/j.bbapap.2005.08.028.
- Pistocchi, C., Tamburini, F., Gruau, G., Ferhi, A., Trevisan, D., & Dorioz, J. M. (2017). Tracing the sources and cycling of phosphorus in river sediments using oxygen isotopes: Methodological adaptations and first results from a case study in France. Water Research, 111, 346–356. https://doi.org/10.1016/j.watres.2016.12.038.
- Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., … Glockner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590–D596. https://doi.org/10.1093/nar/gks1219.
- Rech, J. A., Currie, B. S., Shullenberger, E. D., Dunagan, S. P., Jordan, T. E., Blanco, N., … Houston, J. (2010). Evidence for the development of the Andean rain shadow from a Neogene isotopic record in the Atacama Desert. Chile. Earth and Planetary Science Letters, 292(3–4), 371–382. https://doi.org/10.1016/j.epsl.2010.02.004.
- Rech, J. A., Quade, J., & Hart, W. S. (2003). Isotopic evidence for the source of Ca and S in soil gypsum, anhydrite and calcite in the Atacama Desert. Chile. Geochimica Et Cosmochimica Acta, 67(4), 575–586. https://doi.org/10.1016/S0016-7037(02)01175-4.
- Reddy, K. R., Wetzel, R. G., & Kadlec, R. H. (2005). Biogeochemistry of phosphorus in wetlands. Phosphorus: Agriculture and the environment(phosphorusagric), 263–316.
- Reed, S. C., & Wood, T. E. (2016). Soil phosphorus cycling in tropical soils: an ultisol and oxisol perspective.
- Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahe, F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ, 4, e2584. https://doi.org/10.7717/peerj.2584.
- Scervino, J. M., Mesa, M. P., Della Monica, I., Recchi, M., Moreno, N. S., & Godeas, A. (2010). Soil fungal isolates produce different organic acid patterns involved in phosphate salts solubilization. Biology and Fertility of Soils, 46(7), 755–763. https://doi.org/10.1007/s00374-010-0482-8.
- Scheihing, K. W., Moya, C. E., Struck, U., Lictevout, E., & Troger, U. (2018). Reassessing Hydrological Processes That Control Stable Isotope Tracers in Groundwater of the Atacama Desert (Northern Chile). Hydrology, 5(1), 3. https://doi.org/10.3390/hydrology5010003.
- Schenk, C. J., Viger, R. J., & Anderson, C. P. (1999). Maps showing geology, oil and gas fields, and geological provinces of South America.
- Schindler, D., & Vallentyne, J. (2008). The algal bowl: overfertilization of the world's freshwaters and estuaries Edmonton. In: Alberta, Canada: University of Alberta Press.
- Schotterer, U., Oldfield, F., & Fröhlich, K. (1996). GNIP. Global Network for Isotopes in Precipitation.
- Schulze-Makuch, D., Wagner, D., Kounaves, S. P., Mangelsdorf, K., Devine, K. G., de Vera, J. P., … Zamorano, P. (2018). Transitory microbial habitat in the hyperarid Atacama Desert. Proceedings of the National Academy of Sciences of the United States of America, 115(11), 2670–2675. https://doi.org/10.1073/pnas.1714341115.
- Sharma, S. B., Sayyed, R. Z., Trivedi, M. H., & Gobi, T. A. (2013). Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus, 2, 587. https://doi.org/10.1186/2193-1801-2-587.
- Sheldon, R. P. (1982). Phosphate Rock. Scientific American, 246(6), 45. https://doi.org/10.1038/scientificamerican0682-45.
- Shemesh, A., Kolodny, Y., & Luz, B. (1983). Oxygen Isotope Variations in Phosphate of Biogenic Apatites. 2. Phosphorite Rocks. Earth and Planetary Science Letters, 64(3), 405–416. https://doi.org/10.1016/0012-821x(83)90101-2.
- Shemesh, A., Kolodny, Y., & Luz, B. (1988). Isotope Geochemistry of Oxygen and Carbon in Phosphate and Carbonate of Phosphorite Francolite. Geochimica Et Cosmochimica Acta, 52(11), 2565–2572. https://doi.org/10.1016/0016-7037(88)90027-0.
- Shen, J., Zerkle, A. L., Stueken, E. E., & Claire, M. W. (2019). Nitrates as a Potential N Supply for Microbial Ecosystems in a Hyperarid Mars Analog System. Life, 9(4), 79. https://doi.org/10.3390/life9040079.
10.3390/life9040079 Google Scholar
- Smith, P. H., Tamppari, L. K., Arvidson, R. E., Bass, D., Blaney, D., Boynton, W. V., … Zent, A. P. (2009). H2O at the Phoenix Landing Site. Science, 325(5936), 58–61. https://doi.org/10.1126/science.1172339.
- Smolders, A. J. P., Lucassen, E. C. H. E. T., Bobbink, R., Roelofs, J. G. M., & Lamers, L. P. M. (2010). How nitrate leaching from agricultural lands provokes phosphate eutrophication in groundwater fed wetlands: the sulphur bridge. Biogeochemistry, 98(1–3), 1–7. https://doi.org/10.1007/s10533-009-9387-8.
- Stevenson, A., Burkhardt, J., Cockell, C. S., Cray, J. A., Dijksterhuis, J., Fox-Powell, M., … Hallsworth, J. E. (2015). Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environmental Microbiology, 17(2), 257–277. https://doi.org/10.1111/1462-2920.12598.
- Stomeo, F., Valverde, A., Pointing, S. B., Mckay, C. P., Warren-Rhodes, K. A., Tuffin, M. I., … Cowan, D. A. (2013). Hypolithic and soil microbial community assembly along an aridity gradient in the Namib Desert. Extremophiles, 17(2), 329–337. https://doi.org/10.1007/s00792-013-0519-7.
- Stout, L. M., Joshi, S. R., Kana, T. M., & Jaisi, D. P. (2014). Microbial activities and phosphorus cycling: An application of oxygen isotope ratios in phosphate. Geochimica Et Cosmochimica Acta, 138, 101–116. https://doi.org/10.1016/j.gca.2014.04.020.
- Strauch, G., Oyarzun, J., Fiebig-Wittmaack, M., Gonzalez, E., & Weise, S. M. (2006). Contributions of the different water sources to the Elqui river runoff (northern Chile) evaluated by H/O isotopes. Isotopes in Environmental and Health Studies, 42(3), 303–322. https://doi.org/10.1080/10256010600839707.
- Sun, T., Bao, H. M., Reich, M., & Hemming, S. R. (2018). More than ten million years of hyper-aridity recorded in the Atacama Gravels. Geochimica Et Cosmochimica Acta, 227, 123–132. https://doi.org/10.1016/j.gca.2018.02.021.
- Surma, J., Assonov, S., Herwartz, D., Voigt, C., & Staubwasser, M. (2018). The evolution of O-17-excess in surface water of the arid environment during recharge and evaporation. Scientific Reports, 8, 4972. https://doi.org/10.1038/s41598-018-23151-6.
- Takahashi, K., & Battisti, D. S. (2007). Processes controlling the mean tropical pacific precipitation pattern. Part II: The SPCZ and the southeast pacific dry zone. Journal of Climate, 20(23), 5696–5706. https://doi.org/10.1175/2007jcli1656.1.
- Tamburini, F., Bernasconi, S. M., Angert, A., Weiner, T., & Frossard, E. (2010). A method for the analysis of the delta O-18 of inorganic phosphate extracted from soils with HCl. European Journal of Soil Science, 61(6), 1025–1032. https://doi.org/10.1111/j.1365-2389.2010.01290.x.
- Tamburini, F., Pfahler, V., Bunemann, E. K., Guelland, K., Bernasconi, S. M., & Frossard, E. (2012). Oxygen Isotopes Unravel the Role of Microorganisms in Phosphate Cycling in Soils. Environmental Science & Technology, 46(11), 5956–5962. https://doi.org/10.1021/es300311h.
- Tamburini, F., Pfahler, V., von Sperber, C., Frossard, E., & Bernasconi, S. M. (2014). Oxygen Isotopes for Unraveling Phosphorus Transformations in the Soil-Plant System: A Review. Soil Science Society of America Journal, 78(1), 38–46. https://doi.org/10.2136/sssaj2013.05.0186dgs.
- Tamburini, F., Pistocchi, C., Helfenstein, J., & Frossard, E. (2018). A method to analyse the isotopic composition of oxygen associated with organic phosphorus in soil and plant material. European Journal of Soil Science, 69(5), 816–826. https://doi.org/10.1111/ejss.12693.
- Tapia, J., Gonzalez, R., Townley, B., Oliveros, V., Alvarez, F., Aguilar, G., … Calderon, M. (2018). Geology and geochemistry of the Atacama Desert. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 111(8), 1273–1291. https://doi.org/10.1007/s10482-018-1024-x.
- Tian, H. Q., Chen, G. S., Zhang, C., Melillo, J. M., & Hall, C. A. S. (2010). Pattern and variation of C:N: P ratios in China's soils: a synthesis of observational data. Biogeochemistry, 98(1–3), 139–151. https://doi.org/10.1007/s10533-009-9382-0.
- Trewartha, G. T. (1961). The earth's problem climates (551.59 T817). Retrieved from.
- Tudge, A. P. (1960). A Method of Analysis of Oxygen Isotopes in Orthophosphate - Its Use in the Measurement of Paleotemperatures. Geochimica Et Cosmochimica Acta, 18(1–2), 81–93. https://doi.org/10.1016/0016-7037(60)90019-3.
- Uritskiy, G., Getsin, S., Munn, A., Gomez-Silva, B., Davila, A., Glass, B., … DiRuggiero, J. (2019). Halophilic microbial community compositional shift after a rare rainfall in the Atacama Desert. The ISME Journal, 13(11), 2737–2749. https://doi.org/10.1038/s41396-019-0468-y.
- Urrutia, O., Erro, J., Guardado, I., San Francisco, S., Mandado, M., Baigorri, R., … Garcia-Mina, J. M. (2014). Physico- chemical characterization of humic- metal- phosphate complexes and their potential application to the manufacture of new types of phosphate- based fertilizers. Journal of Plant Nutrition and Soil Science, 177(2), 128–136. https://doi.org/10.1002/jpln.201200651.
- Vangeel, B., Mur, L. R., Ralskajasiewiczowa, M., & Goslar, T. (1994). Fossil Akinetes of Aphanizomenon and Anabaena as Indicators for Medieval Phosphate-Eutrophication of Lake Gosciaz (Central Poland). Review of Palaeobotany and Palynology, 83(1–3), 97–105. https://doi.org/10.1016/0034-6667(94)90061-2.
- Veblen, T. T., Young, K. R., & Orme, A. R. (2015). The physical geography of South America. Oxford: Oxford University Press.
- Vidiella, P. E., Armesto, J. J., & Gutierrez, J. R. (1999). Vegetation changes and sequential flowering after rain in the southern Atacama Desert. Journal of Arid Environments, 43(4), 449–458. https://doi.org/10.1006/jare.1999.0565.
- Vitousek, P. M., Porder, S., Houlton, B. Z., & Chadwick, O. A. (2010). Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecological Applications, 20(1), 5–15. https://doi.org/10.1890/08-0127.1.
- von Sperber, C., Kries, H., Tamburini, F., Bernasconi, S. M., & Frossard, E. J. G. (2014). The effect of phosphomonoesterases on the oxygen isotope composition of phosphate. Geochimica et Cosmochimica Acta, 125, 519–527. https://doi.org/10.1016/j.gca.2013.10.010.
- Walker, T. W., & Syers, J. K. (1976). The fate of phosphorus during pedogenesis. Geoderma, 15(1), 1–19. https://doi.org/10.1016/0016-7061(76)90066-5.
- Weckwerth, G., & Schidlowski, M. (1995). Phosphorus as a potential guide in the search for extinct life on Mars. Advances in Space Research, 15(3), 185–191.
- Xiao, J., Porter, S. C., An, Z. S., Kumai, H., & Yoshikawa, S. (1995). Grain-Size of Quartz as an Indicator of Winter Monsoon Strength on the Loess Plateau of Central China during the Last 130,000-Yr. Quaternary Research, 43(1), 22–29. https://doi.org/10.1006/qres.1995.1003.
- Ye, Y. Z., & Doak, T. G. (2009). A Parsimony Approach to Biological Pathway Reconstruction/Inference for Genomes and Metagenomes. Plos Computational Biology, 5(8), e1000465. https://doi.org/10.1371/journal.pcbi.1000465.
- Yen, A. S., Mittlefehldt, D. W., McLennan, S. M., Gellert, R., Bell, J. F., McSween, H. Y., … Squyres, S. W. (2006). Nickel on Mars: Constraints on meteoritic material at the surface. Journal of Geophysical Research-Planets, 111(E12), 2797. https://doi.org/10.1029/2006je002797.