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Phospholipid biomarkers in Mars-analogous soils of the Atacama Desert

Published online by Cambridge University Press:  12 October 2020

Jianxun Shen Open the ORCID record for Jianxun Shen [Opens in a new window]
Jianxun Shen*
Affiliation:
School of Earth and Environmental Sciences and Centre for Exoplanet Science, University of St Andrews, St Andrews KY16 9AL, Scotland, UK
*
Author for correspondence: Jianxun Shen, E-mail: [email protected]
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Abstract

In Mars-analogous hyperarid soils of the Atacama Desert, phospholipid fatty acids (PLFAs) as the main component of biomembrane play a role in reliably determining viable microbes. PLFA analyses illustrated a rise of the microbial abundance (from 5.0 × 106 to 4.2 × 107 cells g−1) and biodiversity (from 7 to 15 different individual PLFAs) from the north hyperarid core of the Atacama Desert to the southern arid region. Abundant cyclopropyl PLFAs (47.2 ± 4.6%) suggested the resistance to oligotrophic and hypersaline environments by Atacama microbial communities. The southernmost arid site had the highest proportion (8.7%) of eukaryotic and fungal lipid biomarkers. Different precipitations (ranging from 0.7 to 2 mm year−1) in the hyperarid core exerted different effects on microbial biomass, PLFA diversity, bacteria and microeukaryotes. By principal component analysis (cumulative 74.6% of variance), the dominance of PLFA hydroxylation was associated with the microbial viability; bacteria rich in C16:0, C18:0 and C16:1ω9 favoured higher soil conductivity and nitrate; and other PLFAs contributed more to the organic content. Additionally by comparing the ratios of PLFAs to well-preserved organics (e.g., mineral-bound organic carbon and microbial phosphorus), I found that the degradation of PLFAs decreased to a minimum when the mean annual precipitation is lower than 2 mm. These findings may further specify identifiable biomarkers on Mars, if potentially extant Martian microbes possess comparable phospholipid membrane structure.

Keywords

BiomassdegradationGC-MSlipidPLFAstarvationviable
Type
Research Article
Information
International Journal of Astrobiology , Volume 19 , Issue 6 , December 2020 , pp. 505 - 514
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Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Altheide, T, Chevrier, V, Nicholson, C and Denson, J (2009) Experimental investigation of the stability and evaporation of sulfate and chloride brines on Mars. Earth and Planetary Science Letters 282, 69–78.CrossRefGoogle Scholar
Armstrong, A, Valverde, A, Ramond, JB, Makhalanyane, TP, Jansson, JK, Hopkins, DW, Aspray, TJ, Seely, M, Trindade, MI and Cowan, DA (2016) Temporal dynamics of hot desert microbial communities reveal structural and functional responses to water input. Scientific Reports 6, 34434.CrossRefGoogle ScholarPubMed
Azua-Bustos, A, Urrejola, C and Vicuna, R (2012) Life at the dry edge: microorganisms of the Atacama Desert. Febs Letters 586, 2939–2945.CrossRefGoogle Scholar
Azua-Bustos, A, Caro-Lara, L and Vicuna, R (2015) Discovery and microbial content of the driest site of the hyperarid Atacama Desert, Chile. Environmental Microbiology Reports 7, 388–394.CrossRefGoogle ScholarPubMed
Azua-Bustos, A, Gonzalez-Silva, C and Corsini, G (2017) The hyperarid core of the Atacama Desert, an extremely dry and carbon deprived habitat of potential interest for the field of carbon science. Frontiers in Microbiology 8, 993.CrossRefGoogle ScholarPubMed
Azua-Bustos, A, Fairen, AG, Gonzalez-Silva, C, Ascaso, C, Carrizo, D, Fernandez-Martinez, MA, Fernandez-Sampedro, M, Garcia-Descalzo, L, Garcia-Villadangos, M, Martin-Redondo, MP, Sanchez-Garcia, L, Wierzchos, J and Parro, V (2018) Unprecedented rains decimate surface microbial communities in the hyperarid core of the Atacama Desert. Scientific Reports 8, 16706.CrossRefGoogle ScholarPubMed
Azua-Bustos, A, Gonzalez-Silva, C, Fernandez-Martinez, MA, Arenas-Fajardo, C, Fonseca, R, Martin-Torres, FJ, Fernandez-Sampedro, M, Fairen, AG and Zorzano, MP (2019) Aeolian transport of viable microbial life across the Atacama Desert, Chile: implications for Mars. Scientific Reports 9, 11024.CrossRefGoogle ScholarPubMed
Bagaley, DR (2006) Uncovering bacterial diversity on and below the surface of a hyper-arid environment, the Atacama Desert, Chile. Baton Rouge, Louisiana, US: Louisiana State University and Agricultural and Mechanical College.Google Scholar
Balkwill, DL, Leach, FR, Wilson, JT, Mcnabb, JF and White, DC (1988) Equivalence of microbial biomass measures based on membrane lipid and cell-wall components, adenosine-triphosphate, and direct counts in subsurface aquifer sediments. Microbial Ecology 16, 73–84.CrossRefGoogle ScholarPubMed
Bao, T, Gao, L, Wang, S, Yang, X, Ren, W and Zhao, Y (2020) Moderate disturbance increases the PLFA diversity and biomass of the microbial community in biocrusts in the Loess Plateau region of China. Plant and Soil 451, 499–513.CrossRefGoogle Scholar
Ben-David, EA, Zaady, E, Sher, Y and Nejidat, A (2011) Assessment of the spatial distribution of soil microbial communities in patchy arid and semi-arid landscapes of the Negev Desert using combined PLFA and DGGE analyses. FEMS Microbiology Ecology 76, 492–503.CrossRefGoogle ScholarPubMed
Bligh, EG and Dyer, WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.CrossRefGoogle ScholarPubMed
Bonani, G, Friedmann, EI, Ocampo-Friedmann, R, Mckay, CP and Woelfli, W (1988) Preliminary report on radiocarbon dating of cryptoendolithic microorganisms. Polarforschung 58, 199–200.Google ScholarPubMed
Brady, AL, Goordial, J, Sun, HJ, Whyte, LG and Slater, GF (2018) Variability in carbon uptake and (re)cycling in Antarctic cryptoendolithic microbial ecosystems demonstrated through radiocarbon analysis of organic biomarkers. Geobiology 16, 62–79.CrossRefGoogle ScholarPubMed
Brocks, JJ and Banfield, J (2009) Unravelling ancient microbial history with community proteogenomics and lipid geochemistry. Nature Reviews Microbiology 7, 601–9.CrossRefGoogle ScholarPubMed
Carlson, CA and Ingraham, JL (1983) Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans. Applied and Environmental Microbiology 45, 1247–53.CrossRefGoogle ScholarPubMed
Christie, WW (1993) Preparation of ester derivatives of fatty acids for chromatographic analysis. Advances in Lipid Methodology 2, e111.Google Scholar
Connon, SA, Lester, ED, Shafaat, HS, Obenhuber, DC and Ponce, A (2007) Bacterial diversity in hyperarid Atacama Desert soils. Journal of Geophysical Research-Biogeosciences 112, G04S17.CrossRefGoogle Scholar
Dickson, L, Bull, ID, Gates, PJ and Evershed, RP (2009) A simple modification of a silicic acid lipid fractionation protocol to eliminate free fatty acids from glycolipid and phospholipid fractions. Journal of Microbiological Methods 78, 249–254.CrossRefGoogle ScholarPubMed
Dong, HL, Zhang, GX, Jiang, HC, Yu, BS, Chapman, LR, Lucas, CR and Fields, MW (2006) Microbial diversity in sediments of saline Qinghai Lake, China: linking geochemical controls to microbial ecology. Microbial Ecology 51, 65–82.CrossRefGoogle ScholarPubMed
Ewing, SA, Michalski, G, Thiemens, M, Quinn, RC, Macalady, JL, Kohl, S, Wankel, SD, Kendall, C, Mckay, CP and Amundson, R (2007) Rainfall limit of the N cycle on Earth. Global Biogeochemical Cycles 21, GB3009.CrossRefGoogle Scholar
Ewing, SA, Macalady, JL, Warren-Rhodes, K, Mckay, CP and Amundson, R (2008) Changes in the soil C cycle at the arid-hyperarid transition in the Atacama Desert. Journal of Geophysical Research-Biogeosciences 113, G02S90.CrossRefGoogle Scholar
Fan, FQ, Zhang, BY and Morrill, PL (2017) Phospholipid fatty acid (PLFA) analysis for profiling microbial communities in offshore produced water. Marine Pollution Bulletin 122, 194–206.CrossRefGoogle ScholarPubMed
Fernandez-Martinez, MA, Severino, RD, Moreno-Paz, M, Gallardo-Carreno, I, Blanco, Y, Warren-Rhodes, K, Garcia-Villadangos, M, Ruiz-Bermejo, M, Barberan, A, Wettergreen, D, Cabrol, N and Parro, V (2019) Prokaryotic community structure and metabolisms in shallow subsurface of Atacama Desert playas and alluvial fans after heavy rains: repairing and preparing for next dry period. Frontiers in Microbiology 10, 1641.CrossRefGoogle ScholarPubMed
Finstad, K, Probst, AJ, Thomas, BC, Andersen, GL, Demergasso, C, Echeverria, A, Amundson, RG and Banfield, JF (2017) Microbial community structure and the persistence of cyanobacterial populations in salt crusts of the hyperarid Atacama Desert from genome-resolved metagenomics. Frontiers in Microbiology 8, 1435.CrossRefGoogle ScholarPubMed
Fletcher, LE, Conley, CA, Valdivia-Silva, JE, Perez-Montano, S, Condori-Apaza, R, Kovacs, GTA, Glavin, DP and Mckay, CP (2011) Determination of low bacterial concentrations in hyperarid Atacama soils: comparison of biochemical and microscopy methods with real-time quantitative PCR. Canadian Journal of Microbiology 57, 953–963.CrossRefGoogle ScholarPubMed
Frostegard, A and Baath, E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22, 59–65.CrossRefGoogle Scholar
Frostegard, A, Tunlid, A and Baath, E (1991) Microbial biomass measured as total lipid phosphate in soils of different organic content. Journal of Microbiological Methods 14, 151–163.CrossRefGoogle Scholar
Goesmann, F, Brinckerhoff, WB, Raulin, F, Goetz, W, Danell, RM, Getty, SA, Siljestrom, S, Missbach, H, Steininger, H, Arevalo, RD Jr, Buch, A, Freissinet, C, Grubisic, A, Meierhenrich, UJ, Pinnick, VT, Stalport, F, Szopa, C, Vago, JL, Lindner, R, Schulte, MD, Brucato, JR, Glavin, DP, Grand, N, Li, X and Van Amerom, FHW (2017) The Mars Organic Molecule Analyzer (MOMA) instrument: characterization of organic material in Martian sediments. Astrobiology 17, 655–685.CrossRefGoogle ScholarPubMed
Green, CT and Scow, KM (2000) Analysis of phospholipid fatty acids (PLFA) to characterize microbial communities in aquifers. Hydrogeology Journal 8, 126–141.CrossRefGoogle Scholar
Guckert, JB, Hood, MA and White, DC (1986) Phospholipid ester-linked fatty-acid profile changes during nutrient deprivation of vibrio-cholerae – increases in the trans Cis ratio and proportions of cyclopropyl fatty-acids. Applied and Environmental Microbiology 52, 794–801.CrossRefGoogle ScholarPubMed
Gutteridge, JMC (1982) The role of superoxide and hydroxyl radicals in phospholipid peroxidation catalyzed by iron salts. Febs Letters 150, 454–458.CrossRefGoogle Scholar
Hare, VJ, Loftus, E, Jeffrey, A and Ramsey, CB (2018) Atmospheric CO2 effect on stable carbon isotope composition of terrestrial fossil archives. Nature Communications 9, 252.CrossRefGoogle ScholarPubMed
Harvey, HR, Fallon, RD and Patton, JS (1986) The effect of organic matter and oxygen on the degradation of bacterial membrane lipids in marine sediments. Geochimica et Cosmochimica Acta 50, 795–804.CrossRefGoogle Scholar
Hecht, MH, Kounaves, SP, Quinn, RC, West, SJ, Young, SMM, Ming, DW, Catling, DC, Clark, BC, Boynton, WV, Hoffman, J, Deflores, LP, Gospodinova, K, Kapit, J and Smith, PH (2009) Detection of perchlorate and the soluble chemistry of Martian soil at the phoenix lander site. Science (New York, NY) 325, 64–67.CrossRefGoogle Scholar
Huang, G, Li, Y and Su, YG (2015 a) Divergent responses of soil microbial communities to water and nitrogen addition in a temperate desert. Geoderma 251, 55–64.CrossRefGoogle Scholar
Huang, G, Li, Y and Su, YG (2015 b) Effects of increasing precipitation on soil microbial community composition and soil respiration in a temperate desert, Northwestern China. Soil Biology and Biochemistry 83, 52–56.CrossRefGoogle Scholar
Jenkins, SN, Waite, IS, Blackburn, A, Husband, R, Rushton, SP, Manning, DC and O'donnell, AG (2009) Actinobacterial community dynamics in long term managed grasslands. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology 95, 319–334.CrossRefGoogle ScholarPubMed
Jones, DL, Olivera-Ardid, S, Klumpp, E, Knief, C, Huil, PW, Lehndorff, E and Bol, R (2018) Moisture activation and carbon use efficiency of soil microbial communities along an aridity gradient in the Atacama Desert. Soil Biology & Biochemistry 117, 68–71.CrossRefGoogle Scholar
Kaur, A, Chaudhary, A, Kaur, A, Choudhary, R and Kaushik, R (2005) Phospholipid fatty acid – a bioindicator of environment monitoring and assessment in soil ecosystem. Current Science 89, 1103–1112.Google Scholar
Kelly, JJ, Haggblom, MM and Tate, RL (2003) Effects of heavy metal contamination and remediation on soil microbial communities in the vicinity of a zinc smelter as indicated by analysis of microbial community phospholipid fatty acid profiles. Biology and Fertility of Soils 38, 65–71.CrossRefGoogle Scholar
Knief, C, Bol, R, Amelung, W, Kusch, S, Frindte, K, Eckmeier, E, Jaeschke, A, Dunai, T, Fuentes, B and Mörchen, R (2020) Tracing elevational changes in microbial life and organic carbon sources in soils of the Atacama Desert. Global and Planetary Change 184, 103078.CrossRefGoogle Scholar
Kowalenko, CG and Mckercher, RB (1971) Phospholipid P content of Saskatchewan soils. Soil Biology and Biochemistry 3, 243–247.CrossRefGoogle Scholar
Kuhlman, KR, Venkat, P, La Duc, MT, Kuhlman, GM and Mckay, CP (2008) Evidence of a microbial community associated with rock varnish at Yungay, Atacama Desert, Chile. Journal of Geophysical Research-Biogeosciences 113, G04022.CrossRefGoogle Scholar
Kuzyakov, Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biology & Biochemistry 42, 1363–1371.CrossRefGoogle Scholar
Lester, ED, Satomi, M and Ponce, A (2007) Microflora of extreme arid Atacama Desert soils. Soil Biology & Biochemistry 39, 704–708.CrossRefGoogle Scholar
Li, H, Zhang, J, Hu, H, Chen, L, Zhu, Y, Shen, H and Fang, J (2017) Shift in soil microbial communities with shrub encroachment in Inner Mongolia grasslands, China. European Journal of Soil Biology 79, 40–47.CrossRefGoogle Scholar
Liu, Y, Li, X, Xing, Z, Zhao, X and Pan, Y (2013) Responses of soil microbial biomass and community composition to biological soil crusts in the revegetated areas of the Tengger Desert. Applied Soil Ecology 65, 52–59.CrossRefGoogle Scholar
Lu, X, Ma, S, Chen, Y, Yangzom, D and Jiang, H (2018) Squalene found in Alpine grassland soils under a harsh environment in the Tibetan Plateau, China. Biomolecules 8, 154.CrossRefGoogle Scholar
Maier, RM, Drees, KP, Neilson, JW, Henderson, DA, Quade, J and Betancourt, JL (2004) Microbial life in the Atacama Desert. Science 306, 1289–1289.CrossRefGoogle ScholarPubMed
Marsh, KL, Sims, GK and Mulvaney, RL (2005) Availability of urea to autotrophic ammonia-oxidizing bacteria as related to the fate of 14 C-and 15 N-labeled urea added to soil. Biology and Fertility of Soils 42, 137.CrossRefGoogle Scholar
Michalsen, MM, Peacock, AD, Spain, AM, Smithgal, AN, White, DC, Sanchez-Rosario, Y, Krumholz, LR and Istok, JD (2007) Changes in microbial community composition and geochemistry during uranium and technetium bioimmobilization. Applied and Environmental Microbiology 73, 5885–5896.CrossRefGoogle ScholarPubMed
Moss, GP, Smith, PAS and Tavernier, D (1997) IUPAC compendium of chemical terminology. In Burrows, H and Stohner, J (eds). Pure and Applied Chemistry, 2 edn, Research Triangle Park, North Carolina: International Union of Pure and Applied Chemistry, pp. 1307–1375.Google Scholar
Navarro-Gonzalez, R, Rainey, FA, Molina, P, Bagaley, DR, Hollen, BJ, De La Rosa, J, Small, AM, Quinn, RC, Grunthaner, FJ, Caceres, L, Gomez-Silva, B and Mckay, CP (2003) Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science 302, 1018–1021.CrossRefGoogle ScholarPubMed
Olsson, PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiology Ecology 29, 303–310.CrossRefGoogle Scholar
Originlab Corp (2019) Origin(Pro). 2019 ed. Northampton, MA, USA: OriginLab Corporation.Google Scholar
Orlando, J, Alfaro, M, Bravo, L, Guevara, R and 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, 1183–1188.CrossRefGoogle Scholar
Palacio, S, Azorin, J, Montserrat-Marti, G and Ferrio, JP (2014) The crystallization water of gypsum rocks is a relevant water source for plants. Nature Communications 5, 4660.CrossRefGoogle ScholarPubMed
Quideau, SA, Mcintosh, ACS, Norris, CE, Lloret, E, Swallow, MJB and Hannam, K (2016) Extraction and analysis of microbial phospholipid fatty acids in soils. Jove-Journal of Visualized Experiments (114), e54360.Google ScholarPubMed
Ranneklev, SB and Baath, E (2003) Use of phospholipid fatty acids to detect previous self-heating events in stored peat. Applied and Environmental Microbiology 69, 3532–3539.CrossRefGoogle ScholarPubMed
Ruess, L and Chamberlain, PM (2010) The fat that matters: soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biology and Biochemistry 42, 1898–1910.CrossRefGoogle Scholar
Schulze-Makuch, D, Wagner, D, Kounaves, SP, Mangelsdorf, K, Devine, KG, De Vera, JP, Schmitt-Kopplin, P, Grossart, HP, Parro, V, Kaupenjohann, M, Galy, A, Schneider, B, Airo, A, Frosler, J, Davila, AF, Arens, FL, Caceres, L, Cornejo, FS, Carrizo, D, Dartnell, L, Diruggiero, J, Flury, M, Ganzert, L, Gessner, MO, Grathwohl, P, Guan, L, Heinz, J, Hess, M, Keppler, F, Maus, D, Mckay, CP, Meckenstock, RU, Montgomery, W, Oberlin, EA, Probst, AJ, Saenz, JS, Sattler, T, Schirmack, J, Sephton, MA, Schloter, M, Uhl, J, Valenzuela, B, Vestergaard, G, Wormer, L and Zamorano, P (2018) Transitory microbial habitat in the hyperarid Atacama Desert. Proceedings of the National Academy of Sciences of the USA 115, 2670–2675.CrossRefGoogle ScholarPubMed
Shen, J, Zerkle, AL, Stueken, EE and Claire, MW (2019) Nitrates as a potential N supply for microbial ecosystems in a hyperarid mars analog system. Life (Chicago, Ill 9, 79.Google Scholar
Shen, J, Shirey, TB, Wyness, AJ, Claire, MW and Zerkle, AL (2020 a) Spatial and temporal variability of microbial communities and salt distributions across an aridity gradient before and after heavy rains in the Atacama Desert. Preprints 2020020433. doi: 10.20944/preprints202002.0433.v1.Google Scholar
Shen, J, Smith, AC, Claire, MW and Zerkle, AL (2020 b) Unraveling biogeochemical phosphorus dynamics in hyperarid Mars-analogue soils using stable oxygen isotopes in phosphate. Geobiology 00, 1–20.Google Scholar
Shen, J, Zerkle, AL and Claire, MW (in review) Nitrogen cycling and biosignatures in a hyperarid Mars analogue environment.Google Scholar
Shi, W, Becker, J, Bischoff, M, Turco, RF and Konopka, AE (2002) Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination. Applied and Environmental Microbiology 68, 3859–3866.CrossRefGoogle ScholarPubMed
Shirey, TB (2013) Investigating microbial communities and the environmental factors influencing them in manmade and naturally occurring systems (Doctor of Philosophy). Tuscaloosa, Alabama, US: University of Alabama.Google Scholar
Stern, JC, Sutter, B, Freissinet, C, Navarro-Gonzalez, R, Mckay, CP, Archer, PD, Buch, A, Brunner, AE, Coll, P, Eigenbrode, JL, Fairen, AG, Franz, HB, Glavin, DP, Kashyap, S, Mcadam, AC, Ming, DW, Steele, A, Szopa, C, Wray, JJ, Martin-Torres, FJ, Zorzano, MP, Conrad, PG, Mahaffy, PR and Team, MS (2015) Evidence for indigenous nitrogen in sedimentary and aeolian deposits from the Curiosity rover investigations at Gale crater, Mars. Proceedings of the National Academy of Sciences of the USA 112, 4245–4250.CrossRefGoogle ScholarPubMed
Sun, HJ and Friedmann, EI (1999) Growth on geological time scales in the Antarctic cryptoendolithic microbial community. Geomicrobiology Journal 16, 193–202.Google Scholar
Tamburini, F, Pistocchi, C, Helfenstein, J and 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, 816–826.CrossRefGoogle Scholar
Turpin-Jelfs, T, Michaelides, K, Biederman, JA and Anesio, AM (2019) Soil nitrogen response to shrub encroachment in a degrading semi-arid grassland. Biogeosciences 16, 369–381.CrossRefGoogle Scholar
Uritskiy, G, Getsin, S, Munn, A, Gomez-Silva, B, Davila, A, Glass, B, Taylor, J and Diruggiero, J (2019) Halophilic microbial community compositional shift after a rare rainfall in the Atacama Desert. The ISME Journal 13, 2737–2749.CrossRefGoogle ScholarPubMed
Valdivia-Silva, JE, Karouia, F, Navarro-Gonzalez, R and Mckay, C (2016) Microorganisms, organic carbon, and their relationship with oxidant activity in hyper-arid Mars-like soils: implications for soil habitability. Palaios 31, 1–9.CrossRefGoogle Scholar
Vestal, JR (1988) Biomass of the cryptoendolithic microbiota from the Antarctic Desert. Applied and Environmental Microbiology 54, 957–9.CrossRefGoogle ScholarPubMed
Vestal, JR and White, DC (1989) Lipid analysis in microbial ecology – quantitative approaches to the study of microbial communities. Bioscience 39, 535–541.CrossRefGoogle Scholar
Wang, CY, Wu, SJ, Ng, CC, Tzeng, WS and Shyu, YT (2012) Halomonas beimenensis sp. nov., isolated from an abandoned saltern. International Journal of Systematic and Evolutionary Microbiology 62, 3013–7.CrossRefGoogle ScholarPubMed
Wang, F, Michalski, G, Seo, JH and Ge, WS (2014) Geochemical, isotopic, and mineralogical constraints on atmospheric deposition in the hyper-arid Atacama Desert, Chile. Geochimica Et Cosmochimica Acta 135, 29–48.CrossRefGoogle Scholar
Warren-Rhodes, KA, Lee, KC, Archer, SDJ, Cabrol, N, Ng-Boyle, L, Wettergreen, D, Zacny, K, Pointing, SB, Chong, G, Demargasso, C, Foil, G, Tate, CG, Hare, T, Lacap-Bugler, DC, Moersch, J, Tanaka, K, Tebes, C, Vijayarangan, S, Wagner, M, Wang, A, Wei, J and Team, NLAP (2019) Subsurface microbial habitats in an extreme desert mars-analog environment. Frontiers in Microbiology 10, 69.CrossRefGoogle Scholar
Watzinger, A (2015) Microbial phospholipid biomarkers and stable isotope methods help reveal soil functions. Soil Biology and Biochemistry 86, 98–107.CrossRefGoogle Scholar
White, D and Ringelberg, D (2017) Utility of the signature lipid biomarker analysis in determining the in situ viable biomass, community structure, and nutritional/physiologic status of deep subsurface microbiota. In Amy, P (ed). Microbiology of the Terrestrial Deep Subsurface, 1 Edn. New York: CRC Press, pp. 119–136.Google Scholar
White, DC, Stair, JO and Ringelberg, DB (1996) Quantitative comparisons of in situ microbial biodiversity by signature biomarker analysis. Journal of Industrial Microbiology 17, 185–196.CrossRefGoogle Scholar
Wilhelm, MB, Davila, AF, Eigenbrode, JL, Parenteau, MN, Jahnke, LL, Liu, XL, Summons, RE, Wray, JJ, Stamos, BN, O'reilly, SS and Williams, A (2017) Xeropreservation of functionalized lipid biomarkers in hyperarid soils in the Atacama Desert. Organic Geochemistry 103, 97–104.CrossRefGoogle ScholarPubMed
Willers, C (2016) Standardisation and implementation of an optimised method for lipid profiling of microbial communities (PhD). Potchefstroom, South Africa: North-West University (South Africa), Potchefstroom Campus.Google Scholar
Willers, C, Van Rensburg, PJJ and Claassens, S (2015) Phospholipid fatty acid profiling of microbial communities-a review of interpretations and recent applications. Journal of Applied Microbiology 119, 1207–1218.CrossRefGoogle ScholarPubMed
Zelles, L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biology and Fertility of Soils 29, 111–129.CrossRefGoogle Scholar
Ziolkowski, LA, Wierzchos, J, Davila, AF and Slater, GF (2013) Radiocarbon evidence of active endolithic microbial communities in the hyperarid core of the Atacama Desert. Astrobiology 13, 607–616.CrossRefGoogle ScholarPubMed
Zuo, Y, He, C, He, X, Li, X, Xue, Z, Li, X and Wang, S (2020) Plant cover of Ammopiptanthus mongolicus and soil factors shape soil microbial community and catabolic functional diversity in the arid desert in Northwest China. Applied Soil Ecology 147, 103389.CrossRefGoogle Scholar
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