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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Main Authors: Victor Parro, Fernando Puente-Sánchez, Nathalie A. Cabrol, Ignacio Gallardo-Carreño, Mercedes Moreno-Paz, Yolanda Blanco, Miriam García-Villadangos, Cristian Tambley, Virginie C. Tilot, Cody Thompson, Eric Smith, Pablo Sobrón, Cecilia S. Demergasso, Alex Echeverría-Vega, Miguel Ángel Fernández-Martínez, Lyle G. Whyte, Alberto G. Fairén
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Microbiology
Subjects:
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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