Distribution of greenhouse gases in hyper-arid and arid areas of northern Chile and the contribution of the high altitude wetland microbiome (Salar de Huasco, Chile)


Northern Chile harbors different bioclimatic zones including hyper-arid and arid ecosystems and hotspots of microbial life, such as high altitude wetlands, which may contribute differentially to greenhouse gases (GHG) such as carbon dioxide (CO2), methane (CH4) and nitrous oxide (N2O). In this study, we explored ground level GHG distribution and the potential role of a wetland situated at 3800 m.a.s.l, and characterized by high solar radiation < 1600 W m−2, extreme temperature ranges (−12 to 24 °C) and wind stress (< 17 m s−1). The water source of the wetland is mainly groundwater springs, which generates streams and ponds surrounded by peatlands. These sites support a rich microbial aquatic life including diverse bacteria and archaea communities, which transiently form more complex structures, such as microbial mats. In this study, GHG were measured in the water and above ground level air at the wetland site and along an elevation gradient in different bioclimatic areas from arid to hyper-arid zones. The microbiome from the water and sediments was described by high-throughput sequencing 16S rRNA and rDNA genes. The results indicate that GHG at ground level were variable along the elevation gradient potentially associated with different bioclimatic zones, reaching high values at the high Andean steppe and variable but lower values in the Atacama Desert and at the wetland. The water areas of the wetland presented high concentrations of CH4 and CO2, particularly at the spring areas and in air bubbles below microbial mats. The microbial community was rich (> 40 phyla), including archaea and bacteria potentially active in the different matrices studied (water, sediments and mats). Functional microbial groups associated with GHG recycling were detected at low frequency, i.e., < 2.5% of total sequences. Our results indicate that hyper-arid and arid areas of northern Chile are sites of GHG exchange associated with various bioclimatic zones and particularly in aquatic areas of the wetland where this ecosystem could represent a net sink of N2O and a source for CH4 and CO2.

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  1. Aceituno P (1997) Aspectos generales del clima en el altiplano sudamericano. 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 63–69

    Google Scholar 

  2. Aguilar P, Acosta E, Dorador C, Sommaruga R (2016) Large differences in bacterial community composition among three nearby extreme waterbodies of the high Andean plateau. Front Microbiol. https://doi.org/10.3389/fmicb.2016.00976

    Article  PubMed  PubMed Central  Google Scholar 

  3. Albarracín VH, Kurth D, Ordoñez OF et al (2015) High-up: a remote reservoir of microbial extremophiles in central Andean Wetlands. Front Microbiol 6:1404. https://doi.org/10.3389/fmicb.2015.01404

    Article  PubMed  PubMed Central  Google Scholar 

  4. Atlas EL, Gordon LI, Hager SW, Park PK (1971) A practical manual for use of the Technicon AutoAnalyzer in seawater nutrient analyses (revised). Tech. Rep. 215, Department of Oceanography, School of Science, Oregon State University, Corvallis

  5. Barrett BS, Campos DA, Veloso JV, Rondanelli R (2016) Extreme temperature and precipitation events in March 2015 in central and northern Chile. J Geophys Res Atmos 121:4563–4580. https://doi.org/10.1002/2016JD024835

    Article  Google Scholar 

  6. Barros N, Feijóo S, Salgado J et al (2008) The dry limit of microbial life in the Atacama desert revealed by calorimetric approaches. Eng Life Sci 8:477–486. https://doi.org/10.1002/elsc.200820236

    Article  CAS  Google Scholar 

  7. Bridgham SD, Cadillo-Quiroz H, Keller JK, Zhuang Q (2013) Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Glob Chang Biol 19:1325–1346. https://doi.org/10.1111/gcb.12131

    Article  PubMed  Google Scholar 

  8. Cornejo M, Farias L, Paulmier A (2006) Temporal variability in N2O water content and its air-sea exchange in an upwelling area off central Chile (36ºS). Mar Chem 101:85–94

    Article  CAS  Google Scholar 

  9. DeBruyn JM, Nixon LT, Fawaz MN et al (2011) Global biogeography and quantitative seasonal dynamics of Gemmatimonadetes in soil. Appl Environ Microbiol 77:6295–6300. https://doi.org/10.1128/AEM.05005-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Ding WX, Cai ZC (2007) Methane emission from natural wetlands in China: summary of years 1995–2004. Pedosphere 17:475–486. https://doi.org/10.1016/S1002-0160(07)60057-5

    Article  CAS  Google Scholar 

  11. Dorador C, Busekow A, Vila I et al (2008) Molecular analysis of enrichment cultures of ammonia oxidizers from the Salar de Huasco, a high altitude saline wetland in northern Chile. Extremophiles 12:405–414. https://doi.org/10.1007/s00792-008-0146-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Dorador C, Vila I, Remonsellez F et al (2010) Unique clusters of 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

    PubMed  CAS  Article  Google Scholar 

  13. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. 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 12:1–25. https://doi.org/10.1371/journal.pone.0186867

    Article  CAS  Google Scholar 

  15. Farías ME, Rascovan N, Toneatti DM et al (2013) The discovery of stromatolites developing at 3570 m above sea level in a high-altitude volcanic Lake Socompa, Argentinean Andes. PLoS One. https://doi.org/10.1371/journal.pone.0053497

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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 7:1–18. https://doi.org/10.3389/fmicb.2016.01284

    Article  Google Scholar 

  17. Goreau TJ, Kaplan WA, Wofsy SC (1980) Production of NO2 and N2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microbiol 40:526–532

    PubMed  PubMed Central  CAS  Google Scholar 

  18. Hall SJ, Silver WL, Amundson R (2012) Greenhouse gas fluxes from Atacama Desert soils: a test of biogeochemical potential at the Earth’s arid extreme. Biogeochemistry 111:303–315. https://doi.org/10.1007/s10533-011-9650-7

    Article  CAS  Google Scholar 

  19. He GX, Li KH, Liu XJ et al (2014) Fluxes of methane, carbon dioxide and nitrous oxide in an alpine wetland and an alpine grassland of the Tianshan Mountains, China. J Arid Land 6:717–724. https://doi.org/10.1007/s40333-014-0070-0

    Article  Google Scholar 

  20. Hernández KL, Yannicelli B, Olsen LM et al (2016) Microbial activity response to solar radiation across contrasting environmental conditions in Salar de Huasco, northern Chilean altiplano. Front Microbiol 7:1–13. https://doi.org/10.3389/fmicb.2016.01857

    Article  Google Scholar 

  21. Holmes RM, Aminot A, Kérouel R et al (1999) A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 56:1801–1808. https://doi.org/10.1139/f99-128

    Article  CAS  Google Scholar 

  22. Houston J (2006) Variability of precipitation in the Atacama Desert: its causes and hydrological impact. Int J Climatol 26:2181–2198. https://doi.org/10.1002/joc.1359

    Article  Google Scholar 

  23. Intergovernmental Panel on Climate Change (IPCC) (2007) Climate Change 2007: The physical science basis: working group I contribution to the fourth assessment report of the IPCC. Cambridge University Press. http://www.amazon.ca/exec/obidos/redirect?tag=citeulike09-20&amp

  24. Kelley CA, Nicholson BE, Beaudoin CS et al (2014) Trimethylamine and organic matter additions reverse substrate limitation effects on the δ13c values of methane produced in hypersaline microbial mats. Appl Environ Microbiol 80:7316–7323. https://doi.org/10.1128/AEM.02641-14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Kulaev I, Kulakovskaya T (2000) Polyphosphate and phosphate pump. Annu Rev Microbiol 54:709–734. Review https://doi.org/10.1146/annurev.micro.54.1.709

  26. Li T, Zhang Q, Cheng Z et al (2016) Modeling CH4 emissions from natural wetlands on the Tibetan Plateau over the past 60 years: influence of climate change and wetland loss. Atmosphere (Basel) 7:90. https://doi.org/10.3390/atmos7070090

    Article  CAS  Google Scholar 

  27. Löscher CR, Kock A, Könneke M et al (2012) Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 9:2419–2429. https://doi.org/10.5194/bg-9-2419-2012

    Article  CAS  Google Scholar 

  28. Luebert F, Pliscoff P (2006) Sinopsis bioclimática y vegetacional de Chile, 1st edn. Editorial Universitaria, p 323

  29. Majumdar D, Rao P, Maske N (2017) Inter-seasonal and spatial distribution of ground-level greenhouse gases (CO2, CH4, N2O) over Nagpur in India and their management roadmap. Environ Monit Assess 189:121. https://doi.org/10.1007/s10661-017-5829-2

    Article  PubMed  CAS  Google Scholar 

  30. McAuliffe C (1971) Gas chromatographic determination of solutes by multiple phase equilibrium. Chem Technol 1:46–51

    Google Scholar 

  31. Merbt SN, Stahl DA, Casamayor EO et al (2012) Differential photoinhibition of bacterial and archaeal ammonia oxidation. FEMS Microbiol Lett 327:41–46. https://doi.org/10.1111/j.1574-6968.2011.02457.x

    Article  PubMed  CAS  Google Scholar 

  32. Molina V, Hernández K, Dorador C et al (2016) Bacterial active community cycling in response to solar radiation and their influence on nutrient changes in a high-altitude wetland. Front Microbiol 7:1–15. https://doi.org/10.3389/fmicb.2016.01823

    Article  Google Scholar 

  33. Navarro-González R, Rainey FA, Molina P, et al (2003) Mars-like soils in the Atacama Desert, Chile, and the dry limit of microbial life. Science (80-) 302:1018–1021. https://doi.org/10.1126/science.1089143

  34. Olson RJ (1980) Nitrate and ammonium uptake in Antarctic waters1. Limnol Oceanogr 25:1064–1074. https://doi.org/10.4319/lo.1980.25.6.1064

    Article  CAS  Google Scholar 

  35. Quade J, Rech JA, Latorre C et al (2007) Soils at the hyperarid margin: the isotopic composition of soil carbonate from the Atacama Desert, Northern Chile. Geochim Cosmochim Acta 71:3772–3795. https://doi.org/10.1016/j.gca.2007.02.016

    Article  CAS  Google Scholar 

  36. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. https://doi.org/10.1093/nar/gks1219

    PubMed Central  Article  PubMed  Google Scholar 

  37. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Schreiber F, Wunderlin P, Udert KM, Wells GF (2012) Nitric oxide and nitrous oxide turnover in natural and engineered microbial communities: biological pathways, chemical reactions, and novel technologies. Front Microbiol. https://doi.org/10.3389/fmicb.2012.00372

    Article  PubMed  PubMed Central  Google Scholar 

  39. Stevens H, Ulloa O (2008) Bacterial diversity in the oxygen minimum zone of the eastern tropical South Pacific. Environ Microbiol 10:1244–1259. https://doi.org/10.1111/j.1462-2920.2007.01539.x

    Article  PubMed  CAS  Google Scholar 

  40. Torres R, Turner D, Rutllant J, Sobarzo M, Antezana T, González HE (2002) CO2 outgassing off Central Chile (31–30°S) and northern Chile (24–23°S) during austral summer 1997: The effect of wind intensity on the upwelling and ventilation of CO2-rich waters. Deep Sea Res. Part I 49:1413–1429. https://doi.org/10.1016/s09670637(02)00034-1

    Article  CAS  Google Scholar 

  41. Wan W, Li H, Xie H et al (2017) A comprehensive data set of lake surface water temperature over the Tibetan Plateau derived from MODIS LST products 2001–2015. Sci Data 4:170095

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wuebbles DJ, Hayhoe K (2002) Atmospheric methane and global change. 57:177–210

    CAS  Google Scholar 

  43. Zhang H, Sekiguchi Y, Hanada S et al (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163. https://doi.org/10.1099/ijs.0.02520-0

    Article  PubMed  CAS  Google Scholar 

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We are grateful to M.J. Gálvez and D. Kalenitchenko for their technical support, to all the participants of the field trips and particularly to Pedro and Margarita Luca for their hospitality at Salar de Huasco shelter facilities. This work is part of the FONDECYT Project #1140356, #1140179, #11130418, #1171324, #1150891, LIA-MORFUN, COPAS Sur-Austral (PFB-31), INCAR center (1510027), and CONICYT-CNRS 2014 France (PCCI140034).

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Molina, V., Eissler, Y., Cornejo, M. et al. Distribution of greenhouse gases in hyper-arid and arid areas of northern Chile and the contribution of the high altitude wetland microbiome (Salar de Huasco, Chile). Antonie van Leeuwenhoek 111, 1421–1432 (2018). https://doi.org/10.1007/s10482-018-1078-9

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  • Greenhouse gases
  • Methanogens
  • Microbial mat
  • High altitude wetland