, Volume 22, Issue 4, pp 665–673 | Cite as

Microbiome analysis and bacterial isolation from Lejía Lake soil in Atacama Desert

  • Dinka Mandakovic
  • Jonathan Maldonado
  • Rodrigo Pulgar
  • Pablo Cabrera
  • Alexis Gaete
  • Viviana Urtuvia
  • Michael Seeger
  • Verónica Cambiazo
  • Mauricio GonzálezEmail author
Original Paper


As a consequence of the severe climatic change affecting our entire world, many lakes in the Andes Cordillera are likely to disappear within a few decades. One of these lakes is Lejía Lake, located in the central Atacama Desert. The objectives of this study were: (1) to characterize the bacterial community from Lejía Lake shore soil (LLS) using 16S rRNA sequencing and (2) to test a culture-based approach using a soil extract medium (SEM) to recover soil bacteria. This extreme ecosystem was dominated by three phyla: Bacteroidetes, Proteobacteria, and Firmicutes with 29.2, 28.2 and 28.1% of the relative abundance, respectively. Using SEM, we recovered 7.4% of the operational taxonomic units from LLS, all of which belonged to the same three dominant phyla from LLS (6.9% of Bacteroidetes, 77.6% of Proteobacteria, and 15.3% of Firmicutes). In addition, we used SEM to recover isolates from LLS and supplemented the culture medium with increasing salt concentrations to isolate microbial representatives of salt tolerance (Halomonas spp.). The results of this study complement the list of microbial taxa diversity from the Atacama Desert and assess a pipeline to isolate selective bacteria that could represent useful elements for biotechnological approaches.


Atacama Desert Microbiome Soil extract medium (SEM) Isolation and characterization 



This work was supported by Fondecyt Grants 1151384 to MG, 3170523 to DM, 11161083 to RP and 1160802 to VC and Fondap Grant 15090007. JM was supported by CONICYT Ph.D. fellowship 21120313. We are grateful to Myriam González for her technical assistance.

Supplementary material

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  1. Auld RR, Myre M, Mykytczuk NC, Leduc LG, Merritt TJ (2013) Characterization of the microbial acid mine drainage microbial community using culturing and direct sequencing techniques. J Microbiol Methods 93:108–115. CrossRefPubMedGoogle Scholar
  2. Azua-Bustos A, Urrejola C, Vicuna R (2012) Life at the dry edge: microorganisms of the Atacama Desert. FEBS Lett 586:2939–2945CrossRefPubMedGoogle Scholar
  3. Bailey VL, Fansler SJ, Stegen JC, McCue LA (2013) Linking microbial community structure to beta-glucosidic function in soil aggregates. ISME J 7:2044–2053. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bakken LR (1985) Separation and purification of bacteria from soil. Appl Environ Microbiol 49:1482–1487PubMedPubMedCentralGoogle Scholar
  5. Bull AT, Asenjo JA, Goodfellow M, Gomez-Silva B (2016) The Atacama Desert: technical resources and the growing importance of novel microbial diversity. Annu Rev Microbiol 70:215–234. CrossRefPubMedGoogle Scholar
  6. Cabrol N et al (2009) The high-lakes project. J Geophys Res 114:1–20CrossRefGoogle Scholar
  7. Caporaso JG et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cordero RR, Seckmeyer G, Damiani A, Riechelmann S, Rayas J, Labbe F, Laroze D (2014) The world’s highest levels of surface UV. Photochem Photobiol Sci 13:70–81. CrossRefPubMedGoogle Scholar
  9. Crits-Christoph A et al (2013) Colonization patterns of soil microbial communities in the Atacama Desert. Microbiome 1:28. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Davila AF, Hawes I, Ascaso C, Wierzchos J (2013) Salt deliquescence drives photosynthesis in the hyperarid Atacama Desert. Environ Microbiol Rep 5:583–587. CrossRefPubMedGoogle Scholar
  11. Davis KE, Joseph SJ, Janssen PH (2005) Effects of growth medium, inoculum size, and incubation time on culturability and isolation of soil bacteria. Appl Environ Microbiol 71:826–834. CrossRefPubMedPubMedCentralGoogle Scholar
  12. De La Calle I, Cabaleiro N, Lavilla I, Bendicho C (2013) Ultrasound-assisted single extraction tests for rapid assessment of metal extractability from soils by total reflection X-ray fluorescence. J Hazard Mater 260:202–209. CrossRefGoogle Scholar
  13. Demergasso C, Dorador C, Meneses D, Blamey J, Cabrol N, Escudero L, Chong G (2010) Prokaryotic diversity pattern in high-altitude ecosystems of the Chilean Altiplano. J Geophys Res 115:2–14CrossRefGoogle Scholar
  14. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. CrossRefPubMedGoogle Scholar
  16. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Ellis RJ (2004) Artificial soil microcosms: a tool for studying microbial autecology under controlled conditions. J Microbiol Methods 56:287–290CrossRefPubMedGoogle Scholar
  18. Escudero L et al (2007) Investigating microbial diversity and UV radiation impact at the high-altitude lake Aguas Calientes. Proc SPIE 6694:1–12Google Scholar
  19. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631. CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gasc C et al (2015) Capturing prokaryotic dark matter genomes. Res Microbiol 166:814–830. CrossRefPubMedGoogle Scholar
  21. Giovannoni SJR (2000) Evolution, diversity and molecular ecology of marine prokaryotes. In: Kirchman D (ed) Microbial ecology of the oceans. Wiley, New York, pp 47–84Google Scholar
  22. Gómez-Silva B, Rainey FA, Warren-Rhodes K, McKay CP, Navarro-González R (2008) Atacama Desert soil microbiology. In: Dion P, Nautiyal CS (eds) Soil biology series, vol 13. Springer, Berlin, pp 117–132Google Scholar
  23. Grimes DJ, Mills AL, Nealson KH (2000) The importance of viable but nonculturable bacteria in biogeochemistry. In: Colwell RR, Grimes DJ (eds) Nonculturable microorganisms in the environment. ASM Press, Washington, pp 209–227CrossRefGoogle Scholar
  24. Handl S, Dowd SE, Garcia-Mazcorro JF, Steiner JM, Suchodolski JS (2011) Massive parallel 16S rRNA gene pyrosequencing reveals highly diverse fecal bacterial and fungal communities in healthy dogs and cats. FEMS Microbiol Ecol 76:301–310. CrossRefPubMedGoogle Scholar
  25. James N (1958) Soil extract in soil microbiology. Can J Microbiol 4:363–370CrossRefPubMedGoogle Scholar
  26. Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 72:3832–3845. CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Liebeke M, Brozel VS, Hecker M, Lalk M (2009) Chemical characterization of soil extract as growth media for the ecophysiological study of bacteria. Appl Microbiol Biotechnol 83:161–173CrossRefPubMedGoogle Scholar
  29. Liesack W, Janssen PH, Rainey FA, Ward-Rainey N, Stackebrandt E (1997) Microbial diversity in soil: the need for a combined approach using molecular and cultivation techniques. In: van Elsas JD, Trevors JT, Wellington EMH (eds) Modern soil microbiology. Marcel Dekker Inc, New York, pp 375–439Google Scholar
  30. Mandakovic D, Cabrera P, Pulgar R, Maldonado J, Aravena P, Latorre M, Cambiazo V, González M (2015) Complete genome sequence of Microbacterium sp. CGR1, bacterium tolerant to wide abiotic conditions isolated from the Atacama Desert. J Biotechnol 216:149–150. CrossRefPubMedGoogle Scholar
  31. Mandakovic D, Rojas C, Maldonado J, Latorre M, Travisany D, Delage E, Bihouée A, Jean G, Díaz FP, Fernández-Gómez B, Cabrera P, Gaete A, Latorre C, Gutiérrez RA, Maass A, Cambiazo V, Navarrete SA, Eveillard D, González M (2018) Structure and co-occurrence patterns in microbial communities under acute environmental stress reveal ecological factors fostering resilience. Sci Rep 8(1):5875. CrossRefPubMedPubMedCentralGoogle Scholar
  32. McDonald D et al (2012) An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. CrossRefPubMedGoogle Scholar
  33. McKay CP, Friedmann EI, Gomez-Silva B, Caceres-Villanueva L, Andersen DT, 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 3:393–406. CrossRefPubMedGoogle Scholar
  34. Neilson JW et al (2012) Life at the hyperarid margin: novel bacterial diversity in arid soils of the Atacama Desert, Chile. Extremophiles 16:553–566. CrossRefPubMedGoogle Scholar
  35. Nelson DW, Sommers LE (1996) Total Carbon, Organic Carbon and Organic Matter. In: Sparks DL (ed) Methods of Soil Analysis Part 3 Chemical Methods Monograph No 5. Soil Science Society of America, Madison, pp 573–579Google Scholar
  36. Nobu MK, Narihiro T, Rinke C, Kamagata Y, Tringe SG, Woyke T, Liu WT (2015) Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor. ISME J 9:1710–1722. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Parro V et al (2016) Biomarkers and metabolic patterns in the sediments of evolving glacial lakes as a proxy for planetary lake exploration. Astrobiology. PubMedCrossRefGoogle Scholar
  38. Prestel E, Salamitou S, DuBow MS (2008) An examination of the bacteriophages and bacteria of the Namib Desert. J Microbiol 46:364–372. CrossRefPubMedGoogle Scholar
  39. Rettedal EA, Gumpert H, Sommer MO (2014) Cultivation-based multiplex phenotyping of human gut microbiota allows targeted recovery of previously uncultured bacteria. Nat Commun 5:4714. CrossRefPubMedGoogle Scholar
  40. Risacher F, Alonso H, Salazar C (1999) Geoquímica de aguas en cuencas cerradas: I, II y III Regiones—Chile. Tech Rep SIT 51, Conv de Coop DGA-UCN-IRD, Santiago, ChileGoogle Scholar
  41. Rousk J et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. CrossRefPubMedGoogle Scholar
  42. Schloss PD et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Thomas LV, Wimpenny JW (1996) Investigation of the effect of combined variations in temperature, pH, and NaCl concentration on nisin inhibition of Listeria monocytogenes and Staphylococcus aureus. Appl Environ Microbiol 62:2006–2012PubMedPubMedCentralGoogle Scholar
  44. Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46:327–338CrossRefPubMedGoogle Scholar
  45. Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Dinka Mandakovic
    • 1
    • 2
  • Jonathan Maldonado
    • 1
    • 2
  • Rodrigo Pulgar
    • 1
    • 2
    • 3
  • Pablo Cabrera
    • 1
    • 2
  • Alexis Gaete
    • 1
  • Viviana Urtuvia
    • 4
    • 5
  • Michael Seeger
    • 4
  • Verónica Cambiazo
    • 1
    • 2
    • 3
  • Mauricio González
    • 1
    • 2
    • 3
    Email author
  1. 1.Laboratorio de Bioinformática y Expresión GénicaINTA-Universidad de ChileSantiagoChile
  2. 2.Fondap Center for Genome Regulation (CGR)SantiagoChile
  3. 3.Laboratorio de Genómica AplicadaINTA-Universidad de ChileSantiagoChile
  4. 4.Laboratorio de Microbiología Molecular y Biotecnología Ambiental, Departamento de Química, Center for Nanotechnology, Systems Biology and Centro de BiotecnologíaUniversidad Técnica Federico Santa MaríaValparaisoChile
  5. 5.Escuela de Ingeniería Bioquímica, Pontificia Universidad Católica de ValparaísoValparaisoChile

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