Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds
Potential benthic habitats of early Mars lakes, probably oligotrophic, could range from hydrothermal to cold sediments. Dynamic processes in the water column (such as turbidity or UV penetration) as well as in the benthic bed (temperature gradients, turbation, or sedimentation rate) contribute to su...
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Frontiers Media S.A.
2019-05-01
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Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00929/full |
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author | Victor Parro Fernando Puente-Sánchez Nathalie A. Cabrol Nathalie A. Cabrol Ignacio Gallardo-Carreño Mercedes Moreno-Paz Yolanda Blanco Miriam García-Villadangos Cristian Tambley Virginie C. Tilot Virginie C. Tilot Cody Thompson Eric Smith Pablo Sobrón Cecilia S. Demergasso Alex Echeverría-Vega Alex Echeverría-Vega Miguel Ángel Fernández-Martínez Lyle G. Whyte Alberto G. Fairén Alberto G. Fairén |
author_facet | Victor Parro Fernando Puente-Sánchez Nathalie A. Cabrol Nathalie A. Cabrol Ignacio Gallardo-Carreño Mercedes Moreno-Paz Yolanda Blanco Miriam García-Villadangos Cristian Tambley Virginie C. Tilot Virginie C. Tilot Cody Thompson Eric Smith Pablo Sobrón Cecilia S. Demergasso Alex Echeverría-Vega Alex Echeverría-Vega Miguel Ángel Fernández-Martínez Lyle G. Whyte Alberto G. Fairén Alberto G. Fairén |
author_sort | Victor Parro |
collection | DOAJ |
description | Potential benthic habitats of early Mars lakes, probably oligotrophic, could range from hydrothermal to cold sediments. Dynamic processes in the water column (such as turbidity or UV penetration) as well as in the benthic bed (temperature gradients, turbation, or sedimentation rate) contribute to supply nutrients to a potential microbial ecosystem. High altitude, oligotrophic, and deep Andean lakes with active deglaciation processes and recent or past volcanic activity are natural models to assess the feasibility of life in other planetary lake/ocean environments and to develop technology for their exploration. We sampled the benthic sediments (down to 269 m depth) of the oligotrophic lake Laguna Negra (Central Andes, Chile) to investigate its ecosystem through geochemical, biomarker profiling, and molecular ecology studies. The chemistry of the benthic water was similar to the rest of the water column, except for variable amounts of ammonium (up to 2.8 ppm) and nitrate (up to 0.13 ppm). A life detector chip with a 300-antibody microarray revealed the presence of biomass in the form of exopolysaccharides and other microbial markers associated to several phylogenetic groups and potential microaerobic and anaerobic metabolisms such as nitrate reduction. DNA analyses showed that 27% of the Archaea sequences corresponded to a group of ammonia-oxidizing archaea (AOA) similar (97%) to Nitrosopumilus spp. and Nitrosoarchaeum spp. (Thaumarchaeota), and 4% of Bacteria sequences to nitrite-oxidizing bacteria from the Nitrospira genus, suggesting a coupling between ammonia and nitrite oxidation. Mesocosm experiments with the specific AOA inhibitor 2-Phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO) demonstrated an AOA-associated ammonia oxidation activity with the simultaneous accumulation of nitrate and sulfate. The results showed a rich benthic microbial community dominated by microaerobic and anaerobic metabolisms thriving under aphotic, low temperature (4°C), and relatively high pressure, that might be a suitable terrestrial analog of other planetary settings. |
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spelling | doaj.art-0e2dc9098f8146ca97b881d0023474722022-12-22T00:04:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-05-011010.3389/fmicb.2019.00929416736Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-BedsVictor Parro0Fernando Puente-Sánchez1Nathalie A. Cabrol2Nathalie A. Cabrol3Ignacio Gallardo-Carreño4Mercedes Moreno-Paz5Yolanda Blanco6Miriam García-Villadangos7Cristian Tambley8Virginie C. Tilot9Virginie C. Tilot10Cody Thompson11Eric Smith12Pablo Sobrón13Cecilia S. Demergasso14Alex Echeverría-Vega15Alex Echeverría-Vega16Miguel Ángel Fernández-Martínez17Lyle G. Whyte18Alberto G. Fairén19Alberto G. Fairén20Centro de Astrobiología (CSIC-INTA), Madrid, SpainCentro de Astrobiología (CSIC-INTA), Madrid, SpainSETI Institute, Carl Sagan Center, Mountain View, CA, United StatesNASA Ames Research Center, Mountain View, CA, United StatesCentro de Astrobiología (CSIC-INTA), Madrid, SpainCentro de Astrobiología (CSIC-INTA), Madrid, SpainCentro de Astrobiología (CSIC-INTA), Madrid, SpainCentro de Astrobiología (CSIC-INTA), Madrid, SpainCampoalto Operaciones SpA, Santiago, ChileInstituto Español de Oceanografía (IEO), Málaga, SpainMuséum National d’Histoire Naturelle, Paris, FranceSchool of Environmental Sciences, University of Guelph, Guelph, ON, CanadaSETI Institute, Carl Sagan Center, Mountain View, CA, United StatesSETI Institute, Carl Sagan Center, Mountain View, CA, United StatesCentro de Biotecnología, Universidad Católica del Norte, Antofagasta, ChileCentro de Biotecnología, Universidad Católica del Norte, Antofagasta, ChileVicerrectoría de Investigación y Postgrado, Universidad Católica del Maule, Talca, ChileCentro de Astrobiología (CSIC-INTA), Madrid, Spain0Department of Natural Resource Sciences, McGill University, Montreal, QC, CanadaCentro de Astrobiología (CSIC-INTA), Madrid, Spain1Department of Astronomy, Cornell University, Ithaca, NY, United StatesPotential benthic habitats of early Mars lakes, probably oligotrophic, could range from hydrothermal to cold sediments. Dynamic processes in the water column (such as turbidity or UV penetration) as well as in the benthic bed (temperature gradients, turbation, or sedimentation rate) contribute to supply nutrients to a potential microbial ecosystem. High altitude, oligotrophic, and deep Andean lakes with active deglaciation processes and recent or past volcanic activity are natural models to assess the feasibility of life in other planetary lake/ocean environments and to develop technology for their exploration. We sampled the benthic sediments (down to 269 m depth) of the oligotrophic lake Laguna Negra (Central Andes, Chile) to investigate its ecosystem through geochemical, biomarker profiling, and molecular ecology studies. The chemistry of the benthic water was similar to the rest of the water column, except for variable amounts of ammonium (up to 2.8 ppm) and nitrate (up to 0.13 ppm). A life detector chip with a 300-antibody microarray revealed the presence of biomass in the form of exopolysaccharides and other microbial markers associated to several phylogenetic groups and potential microaerobic and anaerobic metabolisms such as nitrate reduction. DNA analyses showed that 27% of the Archaea sequences corresponded to a group of ammonia-oxidizing archaea (AOA) similar (97%) to Nitrosopumilus spp. and Nitrosoarchaeum spp. (Thaumarchaeota), and 4% of Bacteria sequences to nitrite-oxidizing bacteria from the Nitrospira genus, suggesting a coupling between ammonia and nitrite oxidation. Mesocosm experiments with the specific AOA inhibitor 2-Phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO) demonstrated an AOA-associated ammonia oxidation activity with the simultaneous accumulation of nitrate and sulfate. The results showed a rich benthic microbial community dominated by microaerobic and anaerobic metabolisms thriving under aphotic, low temperature (4°C), and relatively high pressure, that might be a suitable terrestrial analog of other planetary settings.https://www.frontiersin.org/article/10.3389/fmicb.2019.00929/fullmicrobiology of deep benthic habitatsAndean lakesdeglaciationammonia oxidationnitrification-denitrificationbenthic sediments |
spellingShingle | Victor Parro Fernando Puente-Sánchez Nathalie A. Cabrol Nathalie A. Cabrol Ignacio Gallardo-Carreño Mercedes Moreno-Paz Yolanda Blanco Miriam García-Villadangos Cristian Tambley Virginie C. Tilot Virginie C. Tilot Cody Thompson Eric Smith Pablo Sobrón Cecilia S. Demergasso Alex Echeverría-Vega Alex Echeverría-Vega Miguel Ángel Fernández-Martínez Lyle G. Whyte Alberto G. Fairén Alberto G. Fairén Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds Frontiers in Microbiology microbiology of deep benthic habitats Andean lakes deglaciation ammonia oxidation nitrification-denitrification benthic sediments |
title | Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds |
title_full | Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds |
title_fullStr | Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds |
title_full_unstemmed | Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds |
title_short | Microbiology and Nitrogen Cycle in the Benthic Sediments of a Glacial Oligotrophic Deep Andean Lake as Analog of Ancient Martian Lake-Beds |
title_sort | microbiology and nitrogen cycle in the benthic sediments of a glacial oligotrophic deep andean lake as analog of ancient martian lake beds |
topic | microbiology of deep benthic habitats Andean lakes deglaciation ammonia oxidation nitrification-denitrification benthic sediments |
url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00929/full |
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