Advertisement

Antonie van Leeuwenhoek

, Volume 111, Issue 8, pp 1361–1374 | Cite as

Microbial community composition and trophic role along a marked salinity gradient in Laguna Puilar, Salar de Atacama, Chile

  • Cristina Dorador
  • Patrick Fink
  • Martha Hengst
  • Gonzalo Icaza
  • Alvaro S. Villalobos
  • Drina Vejar
  • Daniela Meneses
  • Vinko Zadjelovic
  • Lisa Burmann
  • Jana Moelzner
  • Chris Harrod
Original Paper

Abstract

The geological, hydrological and microbiological features of the Salar de Atacama, the most extensive evaporitic sedimentary basin in the Atacama Desert of northern Chile, have been extensively studied. In contrast, relatively little attention has been paid to the composition and roles of microbial communities in hypersaline lakes which are a unique feature in the Salar. In the present study biochemical, chemical and molecular biological tools were used to determine the composition and roles of microbial communities in water, microbial mats and sediments along a marked salinity gradient in Laguna Puilar which is located in the “Los Flamencos” National Reserve. The bacterial communities at the sampling sites were dominated by members of the phyla Bacteroidetes, Chloroflexi, Cyanobacteria and Proteobacteria. Stable isotope and fatty acid analyses revealed marked variability in the composition of microbial mats at different sampling sites both horizontally (at different sites) and vertically (in the different layers). The Laguna Puilar was shown to be a microbially dominated ecosystem in which more than 60% of the fatty acids at particular sites are of bacterial origin. Our pioneering studies also suggest that the energy budgets of avian consumers (three flamingo species) and dominant invertebrates (amphipods and gastropods) use minerals as a source of energy and nutrients. Overall, the results of this study support the view that the Salar de Atacama is a heterogeneous and fragile ecosystem where small changes in environmental conditions may alter the balance of microbial communities with possible consequences at different trophic levels.

Keywords

Halophiles Stable isotopes Fatty acids Microbial mats 16S rRNA gene sequencing Flamingos 

Notes

Acknowledgements

We would like to acknowledge collaborative Grant BMBF-CONICYT N° PCCI1-2043 (BMBF FKZ 01DN13015) and Fondecyt 1140179. Also we deeply acknowledge CONAF and Mr. Nelson Amado for sampling support in Laguna Puilar. We are grateful of Vilma Barrera and Irma Vila for chemical analyses and to Katja Preuss and Daniel Schäfer for help with the fatty acid analyses. Chris Harrod is supported by Nucleo Milenio INVASAL funded by Chile’s government program, Iniciativa Cientifica Milenio from Ministerio de Economia, Fomento y Turismo.

Supplementary material

10482_2018_1091_MOESM1_ESM.docx (1.4 mb)
Supplementary material 1 (DOCX 1458 kb)

References

  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46.  https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x CrossRefGoogle Scholar
  2. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-R, PlymouthGoogle Scholar
  3. Campos V (1997) Microorganismos de ambientes extremos: Salar de Atacama, Chile. In: Charrier R, Aceituno P, Castro M, Llanos A, Raggi LA (eds) El Altiplano: ciencia y conciencia de los Andes. Actas del segundo Simposio internacional de Estudios Altiplánicos, Santiago, pp 143–147Google Scholar
  4. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Dalsgaard J, St John M, Kattner G et al (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefPubMedGoogle Scholar
  6. Demergasso C, Casamayor EO, Chong G et al (2004) Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama Desert, northern Chile. FEMS Microbiol Ecol 48:57–69.  https://doi.org/10.1016/j.femsec.2003.12.013 CrossRefPubMedGoogle Scholar
  7. Demergasso C, Escudero L, Casamayor EO et al (2008) Novelty and spatio–temporal heterogeneity in the bacterial diversity of hypersaline Lake Tebenquiche (Salar de Atacama). Extremophiles 12:491–504.  https://doi.org/10.1007/s00792-008-0153-y CrossRefPubMedGoogle Scholar
  8. Dirección General de Aguas, DGA (1991) Catastro General de usuarios de aguas de los cauces afluentes al Salar de Atacama. Informe final. Tomo 1 - 4Google Scholar
  9. Dorador C, Meneses D, Urtuvia V et al (2009) Diversity of Bacteroidetes in high altitude saline evaporitic basins in northern Chile. J Geophys Res 114:G00D05.  https://doi.org/10.1029/2008JG000837 CrossRefGoogle Scholar
  10. Dorador C, Vila I, Remonsellez F et al (2010) Unique clusters for Archaea in Salar de Huasco, an athalassohaline evaporitic basin of the Chilean Altiplano. FEMS Microbiol Ecol 73:291–302.  https://doi.org/10.1111/j.1574-6941.2010.00891.x Google Scholar
  11. Evershed RP, Bull ID, Corr LT et al (2007) Compound-specific stable isotope analysis in ecology and paleoecology. In: Michener RH, Lajtha K (eds) Stable isotopes in ecology and environmental science, II edn. Blackwell, Oxford, pp 480–540CrossRefGoogle Scholar
  12. Farias ME, Rasuk MC, Gallagher KL et al (2017) Prokaryotic diversity and biogeochemical characteristics of benthic microbial ecosystems at La Brava, a hypersaline lake at Salar de Atacama, Chile. PLoS ONE 12(11):e0186867.  https://doi.org/10.1371/journal.pone.0186867 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Farías ME, Contreras M, Rasuk MC et al (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 18:311–329.  https://doi.org/10.1007/s00792-013-0617-6 CrossRefPubMedGoogle Scholar
  14. Fernandez AB, Rasuk MC, Visscher PT et al (2016) Microbial diversity in sediment ecosystems (evaporites domes, microbial mats, and crusts) of hypersaline Laguna Tebenquiche, Salar de Atacama, Chile. Front Microbiol 7:1284.  https://doi.org/10.3389/fmicb.2016.01284 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ghomi MR, Von Elert E, Borcherding J et al (2014) Fatty acid composition and content of round goby (Neogobius melanostomus Pallas 1814) and monkey goby (Neogobius fluviatilis Pallas 1814), two invasive gobiid species in the lower Rhine River (Germany). J Appl Ichthyol 30(3):527–531.  https://doi.org/10.1111/jai.12312 CrossRefGoogle Scholar
  16. Happel A, Czesny S, Rinchard J et al (2017) Data pre-treatment and choice of resemblance metric affect how fatty acid profiles depict known dietary origins. Ecol Res 32:757–767.  https://doi.org/10.1007/s11284-017-1485-9 CrossRefGoogle Scholar
  17. Imhoff JF, Thiemann B (1991) Influence of salt concentration and temperature on the fatty acid compositions of Ectothiorhodospira and other halophilic phototrophic purple bacteria. Arch Microbiol 156:370-375.  https://doi.org/10.1007/BF00248713 CrossRefGoogle Scholar
  18. Kelley C, Nicholson BE, Beaudoin CS et al (2014) Trimethylamine and organic matter additions reverse substrate limitation effects on the 13C values of methane produced in hypersaline microbial mats. Appl Environ Microbiol 80(23):7316–7323.  https://doi.org/10.1128/AEM.02641-14 CrossRefPubMedPubMedCentralGoogle Scholar
  19. King G (2015) Carbon monoxide as a metabolic energy source for extremely halophilic microbes: implications for microbial activity in Mars regolith. Proc Natl Acad Sci USA 112(14):4465–4470.  https://doi.org/10.1073/pnas.1424989112 CrossRefPubMedGoogle Scholar
  20. Larsen T, Taylor DL, Leigh MB et al (2009) Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90:3526–3535.  https://doi.org/10.1890/08-1695.1 CrossRefPubMedGoogle Scholar
  21. Lizama C, Monteoliva-Sanchez M, Suárez-García A et al (2002) Halorubrum tebenquichense sp. nov., a novel halophilic archaeon isolated from the Atacama Saltern, Chile. Int J Syst Evol Microbiol 52:149–155.  https://doi.org/10.1099/00207713-52-1-149 CrossRefPubMedGoogle Scholar
  22. Mardones L (1997) Flux et evolution des solutions salines dans les systemes hidrologiques des salars d’ Ascotan et d’ Atacama. These de Doctorat en Sciences de la Terre, Universitè et ParisGoogle Scholar
  23. McCutchan JH, Lewis WM, Kendall C et al (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390.  https://doi.org/10.1034/j.1600-0706.2003.12098.x CrossRefGoogle Scholar
  24. McDuff S, King GM, Neupane S et al (2016) Isolation and characterization of extremely halophilic CO-oxidizing Euryarchaeota from hypersaline cinders, sediments and soils and description of a novel CO oxidizer, Haloferax namakaokahaiae Mke2.3T, sp. nov. FEMS Microbiol Ecol 92(4):fiw028.  https://doi.org/10.1093/femsec/fiw028 CrossRefPubMedGoogle Scholar
  25. Middelburg JJ (2014) Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences 11:2357–2371.  https://doi.org/10.5194/bg-11-2357-2014 CrossRefGoogle Scholar
  26. Mizutani H, Fukuda M, Kabaya Y (1992) 13C and 15N enrichment factors of feathers of 11 species of adult birds. Ecology 73:1391–1395.  https://doi.org/10.2307/1940684 CrossRefGoogle Scholar
  27. Ortiz C, Aravena R, Briones E et al (2013) Sources of surface water for the Soncor ecosystem, Salar de Atacama basin, northern Chile. Hydrolog Sci J 59:336–350.  https://doi.org/10.1080/02626667.2013.829231 CrossRefGoogle Scholar
  28. Paliy O, Shankar V (2016) Application of multivariate statistical techniques in microbial ecology. Mol Ecol 25:1032–1057.  https://doi.org/10.1111/mec.13536 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Pedrós-Alió C (2012) The rare bacterial biosphere. Ann Rev Mar Sci 4:449–466.  https://doi.org/10.1146/annurev-marine-120710-100948 CrossRefGoogle Scholar
  30. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320.  https://doi.org/10.1146/annurev.es.18.110187.001453 CrossRefGoogle Scholar
  31. Prado B, Lizama C, Aguilera M et al (2006) Chromohalobacter nigrandesensis sp. nov., a moderately halophilic, Gram-negative bacterium isolated from Lake Tebenquiche on the Atacama Saltern, Chile. Int J Syst Evol Microbiol 56:647–651.  https://doi.org/10.1099/ijs.0.63983-0 CrossRefPubMedGoogle Scholar
  32. Quillaguamán J, Delgado O, Mattiasson B et al (2004) Chromohalobacter sarecensis sp. nov., a psychrotolerant moderate halophile isolated from the saline Andean region of Bolivia. Int J Syst Evol Microbiol 54:1921–1926.  https://doi.org/10.1099/ijs.0.63153-0 CrossRefPubMedGoogle Scholar
  33. Rasuk MC, Fernández AB, Kurth D et al (2016) Bacterial diversity in microbial mats and sediments from the Atacama Desert. Microb Ecol 71:44–56.  https://doi.org/10.1007/s00248-015-0649-9 CrossRefPubMedGoogle Scholar
  34. Risacher F, Alonso H (1996) Geoquímica del Salar de Atacama, parte 2: evolución de las aguas. Rev Geol Chile 23(2):123–134.  https://doi.org/10.5027/andgeoV23n2-a02 CrossRefGoogle Scholar
  35. Risacher F, Alonso H, Salazar C (1999) Geoquímica de Aguas en Cuencas Cerradas: I, II y III Regiones - Chile. Volumen III: Estudio de Cuencas de la II Región. Convenio de Cooperación DGA – UCN – IRD (S.I.T. Nº 51)Google Scholar
  36. Thiel V, Tank M, Neulinger SC et al (2010) Unique communities of anoxygenic phototrophic bacteria in saline lakes of Salar de Atacama (Chile): evidence for a new phylogenetic lineage of phototrophic Gammaproteobacteria from pufLM gene analyses. FEMS Microbiol Ecol 74:510–522.  https://doi.org/10.1111/j.1574-6941.2010.00966.x CrossRefPubMedGoogle Scholar
  37. Zúñiga LR, Campos V, Pinochet H et al (1991) A limnological reconnaissance of lake Tebenquiche, Salar de Atacama, Chile. Hydrobiologia 210:19–24.  https://doi.org/10.1007/BF00014320 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Laboratorio de Complejidad Microbiana y Ecología Funcional, Instituto AntofagastaUniversidad de AntofagastaAntofagastaChile
  2. 2.Departamento de Biotecnología, Facultad de Ciencias del Mar y Recursos BiológicosUniversidad de AntofagastaAntofagastaChile
  3. 3.Centre for Biotechnology & Bioengineering (CeBiB)SantiagoChile
  4. 4.Workgroup Aquatic Chemical EcologyUniversity of Cologne, Cologne BiocenterCologneGermany
  5. 5.Laboratory of Molecular Ecology and Applied Microbiology, Departamento de Ciencias FarmacéuticasUniversidad Católica del NorteAntofagastaChile
  6. 6.Instituto de Ciencias Naturales Alexander von Humboldt, Facultad de Ciencias del Mar y Recursos BiológicosUniversidad de AntofagastaAntofagastaChile
  7. 7.Núcleo Milenio INVASALConcepciónChile
  8. 8.Marine Microbiology, GEOMAR HelmholtzCentre for Ocean Research KielKielGermany

Personalised recommendations