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A Test in a High Altitude Lake of a Multi-Parametric Rapid ORIGINAL RESEARCH published: 18 June 2019 doi: 10.3389/fenvs.2019.00070 A Test in a High Altitude Lake of a Multi-Parametric Rapid Methodology for Assessing Life in Liquid Environments on Planetary Bodies: A Potential New Freshwater Polychaete Tubeworm Community Edited by: Virginie C. Tilot 1,2*, Nathalie A. Cabrol 3,4, Victor Parro 5, Alberto G. Fairén 5,6, Henderson James Cleaves, Rupert F. G. Ormond 7,8,9, Enrique Moreno-Ostos 10, Nieves Lopez-Gonzalez 2, Tokyo Institute of Technology, Japan Fabián A. Figueroa 11, Ignacio Gallardo-Carreño 5, Eric W. Smith 3, Pablo Sobrón 3, Reviewed by: Cecilia Demergasso 12, Cristian Tambley 13 and Julie Robidart 14 Dirk De Beer, Max-Planck-Gesellschaft 1 Museum National d’Histoire Naturelle, PATRINAT, Paris, France, 2 Instituto Español de Oceanografía (IEO), Málaga, Spain, (MPG), Germany 3 Carl Sagan Center, SETI Institute, Mountain View, CA, United States, 4 NASA Ames Research Center, Moffett Field, CA, Amy Michele Grunden, United States, 5 Centro de Astrobiología (CSIC-INTA), Madrid, Spain, 6 Department of Astronomy, Cornell University, Ithaca, North Carolina State University, NY, United States, 7 Centre for Marine Biodiversity and Biotechnology, Heriot-Watt University, Edinburgh, United Kingdom, United States 8 Faculty of Marine Sciences, King Abdulaziz University, Jeddah, Saudi Arabia, 9 Marine Conservation International, Edinburgh, United Kingdom, 10 Department of Ecology and Geology, University of Málaga, Málaga, Spain, 11 Laboratorio de *Correspondence: Química de Productos Naturales, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Virginie C. Tilot Concepción, Chile, 12 Centro de Biotecnología, Universidad Católica de Norte, Antofagasta, Chile, 13 Campoalto Operaciones [email protected]; SpA, Santiago, Chile, 14 Ocean Technology and Engineering, National Oceanography Centre, Southampton, United Kingdom [email protected] Specialty section: On our planet, aqueous environments such as deep sea or high-altitude aphotic lakes, This article was submitted to subject to present or past volcanic activity and active deglaciation, may provide analogs Microbiological Chemistry and Geomicrobiology, to the aqueous environments found on such planetary bodies as Europa, Titan or a section of the journal Enceladus. We report here on the methodologies and technologies tested in Laguna Frontiers in Environmental Science Negra, a high altitude lake in the Central Andes, Chile, for exploring and assessing the Received: 06 December 2018 Accepted: 09 May 2019 presence of life within planetary lakes or interior oceans. We adopted a multi-parametric Published: 18 June 2019 Rapid Ecological Assessment (REA) approach centered around collecting video Citation: imagery (by an Underwater Imaging System) and sampling benthic sediments Tilot VC, Cabrol NA, Parro V, (for sedimentological, biological and geochemical analysis) to depths of 272 m, to Fairén AG, Ormond RFG, Moreno-Ostos E, Lopez-Gonzalez N, complement physico-chemical sampling of the water column and collection of shallow Figueroa FA, Gallardo-Carreño I, sediments for microbiological analysis (reported in separate publications). This enabled Smith EW, Sobrón P, Demergasso C, Tambley C and Robidart J (2019) us to classify and assess the apparent status of benthic habitats, based on substrata and A Test in a High Altitude Lake of a environmental characteristics, together with floral and faunal community characteristics Multi-Parametric Rapid Methodology and bioturbation artifacts. Video imagery showed that the lower water column was for Assessing Life in Liquid Environments on Planetary Bodies: A characterized by a variably intense sestonic flux of particles and debris, among which Potential New Freshwater Polychaete were planktonic organisms such as ostracods, copepods, and possibly cladocerans. Tubeworm Community. Front. Environ. Sci. 7:70. Sediment analysis revealed at all depths abundant diatom frustules, mainly of an doi: 10.3389/fenvs.2019.00070 acidophile pennade diatom Pinnularia acidicola, amid vegetal debris likely originating Frontiers in Environmental Science | www.frontiersin.org 1 June 2019 | Volume 7 | Article 70 Tilot et al. Assessment of Life in Liquid Planetary Environments from littoral macrophytes. Video imagery showed that the lakebed was partly covered by microbial mats and depositional matter and harbored an unexpectedly rich assortment of macrofauna, including sponges, tubificid worms, flatworms, bivalves and crustaceans. Various forms of bioturbation were also encountered, some with the animals in the tracks. Most notably, at the deepest site, a previously undescribed faunal feature was evident, apparently formed by a mat-like community of several layers of what appeared to be polychaete tubeworms, possibly of the family Siboglinidae. It is hypothesized that the hydrothermal activity observed in the region may supply the compounds able to support the deep-water microrganisms from which such tubeworms typically gain sustenance. Such processes could be present on other deep and aphotic liquid-water-bearing planetary bodies. Keywords: planetary exploration, rapid environmental assessment, life detection, macrophytes, diatoms, high altitude lakes, andes environment, tubeworm communities INTRODUCTION of organics (Sobron et al., 2013), and (iii) investigation of the microbiology of both benthic sediments (Parro et al., 2018) and Interpretation of images taken by the Hubble Space Telescope the water column (Echeverría-Vega et al., 2018). Complementary would suggest that plumes of water erupt from Jupiter’s icy work involved the analysis, using a Rapid Ecological Assessment moon Europa (Roth et al., 2014) and from Enceladus, one of (REA) approach, of video imagery collected from all depths, Saturn’s moons (Postberg et al., 2011; Thomas et al., 2016). supplemented by the collection of water-sediment samples from These plumes are thought to be material ejected from internal the bottom of the lake for sedimentological, biological and oceans or lakes existing beneath an external ice crust as a result geochemical analysis (Tilot, 2014a). The latter supplemented of hydrothermal activity, as suggested by Hsu et al. (2015), previous microbiological analysis of bottom sediments using (a) Postberg et al. (2011) and Thomas et al. (2016) for Enceladus DNA extraction, cloning and sequencing, (b) ammonia oxidizing and Vance et al. (2007) for small ocean planets. Consequently activity and nitrate and sulfate evolution testing in separate other authors have envisioned that Europa’s inner oceans might mesocosm experiments, and (c) microarray immunoassays contain a variety of potentially life-supporting environments with an immunological Life Detector Chip (LDChip) with a (Chyba and Phillips, 2002; Pappalardo et al., 2013; Phillips and 300-antibody microarray biosensor specifically developed for Pappalardo, 2014), ranging from hydrothermal vents to cold planetary exploration and environmental monitoring (Parro liquid brines (Lowell and DuBose, 2005; Russell et al., 2017). et al., 2018, 2019). Here we present the main results of the In addition, an internal ocean of salty water is thought to exist REA work directed at to a multi-parametric assessment of the on Titan, as revealed by its rotation (Lorenz et al., 2008), while lake ecosystem directed at understanding the structure and the presence of liquid methane lakes on its surface is confirmed functioning of the lake ecosystem. by data received by the Cassini-Huygens spacecraft (Sagan and A separate issue that it was intended for the PLL to Dermott, 1982; Lorenz et al., 2008; Lunine and Atreya, 2008; address was the concern about the capacity of high-altitude Moriconi et al., 2010). lake systems to buffer the potential effects of nutrient addition NASA’s Europa Lander Project has as its aim the detection anticipated as a consequence of either periodic deglaciation of life or its fingerprints in the internal ocean system of or the deglaciation associated with current climate change Europa, through exploration and sampling of potential ocean CONAMA (2007). Glacier surface areas have diminished by more life-forms or of biotic material that might have accumulated than 30% in the past 50 years, a trend that has accelerated through time (Pappalardo et al., 2013; Russell et al., 2017). recently (Rabatel et al., 2011), including for the Echaurren With this purpose in mind the Planetary Lake Lander (PLL) Glacier close to Laguna Negra (Escobar et al., 2000; Carrasco project (Cabrol et al., 2012, 2014; Pedersen et al., 2015) selected et al., 2005; Rabatel et al., 2011). Increased nutrient input to the extreme environment of Laguna Negra, a glacier lake in high altitude lakes has been anticipated as a result of either the southern volcanic zone of the central Chilean Andes, in increased input of water as a result of glacial melt (Roig order to test methods and technologies suitable for work in et al., 2001; Le Quesne et al., 2009), or as a consequence extreme planetary aqueous environments. The PLL campaign of melting of the upstream permafrost within the catchment undertaken in 2013 involved a complete investigation of the (Rogora et al., 2008; Salerno et al., 2016). Such alterations may lake ecosystem, including (i) collection of data on bathymetry lead to oligotrophic lakes becoming more eutrophic (Lyons (Cabrol et al., 2015), temperature and light distribution levels et al., 2006; Modenutti et al., 2013) and to linked changes in through the whole water column (Rose et al., 2014;
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