Biomarkers and Metabolic Patterns in the Sediments of Evolving Glacial Lakes As a Proxy for Planetary Lake Exploration
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ASTROBIOLOGY Volume 18, Number 5, 2018 ª Mary Ann Liebert, Inc. DOI: 10.1089/ast.2015.1342 Biomarkers and Metabolic Patterns in the Sediments of Evolving Glacial Lakes as a Proxy for Planetary Lake Exploration Vı´ctor Parro,1 Yolanda Blanco,1 Fernando Puente-Sa´nchez,1 Luis A. Rivas,1 Mercedes Moreno-Paz,1 Alex Echeverrı´a,2 Guillermo Chong-Dı´az,2 Cecilia Demergasso,2 and Nathalie A. Cabrol3 Abstract Oligotrophic glacial lakes in the Andes Mountains serve as models to study the effects of climate change on natural biological systems. The persistent high UV regime and evolution of the lake biota due to deglaciation make Andean lake ecosystems potential analogues in the search for life on other planetary bodies. Our objective was to identify microbial biomarkers and metabolic patterns that represent time points in the evolutionary history of Andean glacial lakes, as these may be used in long-term studies as microscale indicators of climate change processes. We investigated a variety of microbial markers in shallow sediments from Laguna Negra and Lo Encan˜ado lakes (Regio´n Metropolitana, Chile). An on-site immunoassay-based Life Detector Chip (LDChip) revealed the presence of sulfate-reducing bacteria, methanogenic archaea, and exopolymeric substances from Gammaproteobacteria. Bacterial and archaeal 16S rRNA gene sequences obtained from field samples confirmed the results from the immunoassays and also revealed the presence of Alpha-, Beta-, Gamma-, and Deltaproteo- bacteria, as well as cyanobacteria and methanogenic archaea. The complementary immunoassay and phylogenetic results indicate a rich microbial diversity with active sulfate reduction and methanogenic activities along the shoreline and in shallow sediments. Sulfate inputs from the surrounding volcanic terrains during deglaciation may explain the observed microbial biomarker and metabolic patterns, which differ with depth and between the two lakes. A switch from aerobic and heterotrophic metabolisms to anaerobic ones such as sulfate reduction and methanogenesis in the shallow shores likely reflects the natural evolution of the lake sediments due to deglaciation. Hydrodynamic deposition of sediments creates compartmentalization (e.g., sediments with different structure and composition surrounded by oligotrophic water) that favors metabolic transitions. Similar phenomena would be expected to occur on other planetary lakes, such as those of Titan, where watery niches fed by depositional events would be surrounded by a ‘‘sea’’ of hydrocarbons. Key Words: Glacier lakes—Sedimentation—Prokaryotic metabolisms and biomarkers—Deglaciation—Life detection—Planetary exploration. Astrobiology 18, 586–606. 1. Introduction of the world’s largest sources of glacial water, which includes mountain glaciers, ice, and snowfields that are receding rap- ith global temperature rising, ice worldwide re- idly (Haeberli et al., 2002; Le Quesne and Acun˜a, 2003; Downloaded by Consejo Superior De Investigaciones Cientificas CSIC from www.liebertpub.com at 07/22/18. For personal use only. Wtreats and thins. It is projected that many low-altitude Coudrain et al., 2005; Bradley et al., 2006; Rivera et al., 2007; glaciers could disappear within 20 years (IPCC, 2007). Long- Vuille et al., 2008; Le Quesne et al., 2009). Glacial lakes and term, multiproxy studies in regions between 33°S and 36°Sin their sediments are highly sensitive temporal markers of en- Chile and Argentina have shown a mean frontal retreat of vironmental variability, which in turn affects their biota. between -50 and -9my-1, thinning rates between 0.76 and Microbiological studies of oligotrophic Andean lakes have 0.56 m y-1, and a mean ice area reduction of 3% since 1955 shown that changes in the water column occur in association (Roig et al., 2000; Le Quesne and Acun˜a, 2003; Lara et al., with fluctuations in water transparency or turbidity during de- 2005; Vuille, 2006; Le Quesne et al., 2009). The IPCC (2007) glaciation (Modenutti et al., 2012). During early deglaciation lists the Central and Southern Andean countries as particu- (phase 1), the high silt content of water protects microorgan- larly vulnerable (Painter, 2007). Among those, Chile has one isms from the high UV that occurs at the higher altitudes of 1Department of Molecular Evolution, Centro de Astrobiologı´a (INTA-CSIC), Madrid, Spain. 2Centro de Biotecnologı´a ‘‘Profesor Alberto Ruiz,’’ Universidad Cato´lica del Norte, Antofagasta, Chile. 3The SETI Institute, Carl Sagan Center, Mountain View, California, and NASA Ames Research Center, Moffett Field, California, USA. 586 BIOMARKERS IN EVOLVING GLACIAL LAKES 587 glacial lakes. With time, however, as glaciers continue to re- past 10 years and has been implemented—along with the cede, the meltwater discharge and sediment load into the lakes Signs of Life Detector (SOLID) instrument—for in situ detec- decrease (phase 2), and the transparency and UV levels of the tion of biomarkers (Parro et al., 2008, 2011b). The LDChip has water column increase. A comparative study of six Andean been used for in situ detection of prokaryotes and biomarker ultra-oligotrophic lakes characterized by low-phosphorus profiling in different extreme environments that include the concentrations revealed that high photosynthetically active acidic iron-rich sediments of the Rı´o Tinto in Spain (Parro et al., radiation (PAR), UVA, and UVB forced planktonic organisms 2008, 2011c; Puente-Sa´nchez et al., 2014), subsurface sedi- into deeper layers of the water column (Callieri et al., 2007). In ments (down to 5 m depth) cored in the hypersaline Atacama contrast, the microbial diversity (i.e., picocyanobacterial as- Desert (Parro et al., 2011a; Ferna´ndez-Remolar et al., 2013), semblages) of such lakes may remain high, a finding attributed and the surface and permafrost (down to 4.2 m) sediments to habitat fragmentation generated by geographic barriers, drilled on Deception Island in Antarctica (Blanco et al., 2012). which resulted in rapid speciation (Caravati et al., 2010). The LDChip results reported here reveal a rich geochemistry in The combination of environmental and climate factors can Andean lakes that is capable of sustaining an active anaerobic also affect the biodiversity of microbial communities in gla- metabolism and broad microbial diversity. Such data also cial lake sediments. Leo´n et al. (2012) reported differences in provides a baseline for further monitoring to understand the the metabolic activity and structural and functional compo- evolution of deglaciation as recorded in glacial lake sediments. sition of bacterial communities between the sediments of three Patagonian Chilean oligotrophic lakes of quaternary 2. Geological Setting glacial origin. They attributed these differences to the unique geomorphological pattern of each lake due to both local (e.g., Laguna Negra and Lo Encan˜ado are located on the south slope volcanic activity) and global (climate change) disturbances. of the Echaurren glacier watershed in the Central Andes of Chile Such examples illustrate how the microbial communities (33.65S, 70.13W; Fig. 1). Monitoring these lakes over time that live in the water column and sediments of glacial lakes and would allow for characterization of their prokaryotic diversity, reservoirs reflect their environmental setting and geochemical physical processes, and spatiotemporal changes. The two lakes input. Although lower and more acidic precipitation, increased are part of a complex of freshwater resources in the Santiago area temperature, and snow melting that accompanies deglaciation that includes El Yeso lake to the east, which is damned (on its strongly affect the dissolved organic carbon concentration of southern end). Though Laguna Negra and Lo Encan˜ado were glacial lakes (Beniston et al., 1997; Sala et al., 2000; Wil- connected by a human-made overflow tunnel, the lake level of liamson et al., 2009), microbes ultimately control the carbon Laguna Negra has decreased enough that the two lakes have cycle of glacial lakes through metabolic processes, such as been isolated from each other for at least the past 5 years. fermentation of complex organic matter or the production of Both lakes are located in the same catchment area (up to methane (Wadham et al.,2008). 4600 m in elevation), yet they are fed by two distinct stream Oligotrophic water, characterized by low organic carbon systems and have contrasting physical characteristics: Laguna and microbial biomass, is a general feature of glacial Andean Negra is a large (6.1 · 1.7 km) and deep (276 m in 2013) lake lakes. Although some works have reported on the microbial located at 2700 m above sea level, whereas Lo Encan˜ado is content, photosynthetic activity, and geochemistry of the water a smaller, 980 · 635 m wide, and 45 m deep lake located at column of these lakes, very little is actually known about their 2492 m elevation. sediments, which may reveal key aspects of the evolution of The watershed area of the lakes is composed primarily of these important ecosystems with regard to ecology, water re- volcanic constructs and basalt and andesite deposits that sources (e.g., for human consumption), and the evolution of were covered by modern glacial deposits from the receding glacier lakes at planetary scales. Determining whether there are Echaurren glacier, which now lies above the lakes at 3500 m predictable microbial successions or key biomarkers that might elevation. Lahar deposits mark recent to modern interactions be indicative of the progressive evolution of glacial lake