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Geomicrobiological Heterogeneity of Lithic Habitats in the Extreme Environment of Antarctic Nunataks: a Potential Early Mars Analog

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Geomicrobiological Heterogeneity of Lithic Habitats in the Extreme Environment of Antarctic Nunataks: a Potential Early Mars Analog ORIGINAL RESEARCH published: 02 July 2021 doi: 10.3389/fmicb.2021.670982 Geomicrobiological Heterogeneity of Lithic Habitats in the Extreme Environment of Antarctic Nunataks: A Potential Early Mars Analog Miguel Ángel Fernández-Martínez 1,2*, Miriam García-Villadangos 1, Mercedes Moreno-Paz 1, Valentin Gangloff 1, Daniel Carrizo 1, Yolanda Blanco 1, Sergi González 3, Laura Sánchez-García 1, Olga Prieto-Ballesteros 1, Ianina Altshuler 2, Lyle G. Whyte 2, Victor Parro 1 and Alberto G. Fairén 1,4 Edited by: 1 Centro de Astrobiología, CSIC-INTA, Madrid, Spain, 2 Department of Natural Resource Sciences, Faculty of Agricultural and Alberto Robador, Environmental Sciences, McGill University, Sainte-Anne-de-Bellevue, QC, Canada, 3 Antarctic Group, Agencia Estatal de University of Southern California, Meteorología, Barcelona, Spain, 4 Department of Astronomy, Cornell University, Ithaca, NY, United States Los Angeles, United States Reviewed by: Nunataks are permanent ice-free rocky peaks that project above ice caps in polar regions, Peter Convey, British Antarctic Survey (BAS), thus being exposed to extreme climatic conditions throughout the year. They undergo United Kingdom extremely low temperatures and scarcity of liquid water in winter, while receiving high incident Daniel Colman, and reflected (albedo) UVA-B radiation in summer. Here, we investigate the geomicrobiology Montana State University, United States of the permanently exposed lithic substrates of nunataks from Livingston Island (South *Correspondence: Shetlands, Antarctic Peninsula), with focus on prokaryotic community structure and their Miguel Ángel Fernández-Martínez main metabolic traits. Contrarily to first hypothesis, an extensive sampling based on different [email protected]; [email protected] gradients and multianalytical approaches demonstrated significant differences for most geomicrobiological parameters between the bedrock, soil, and loose rock substrates, which Specialty section: overlapped any other regional variation. Brevibacillus genus dominated on bedrock and soil This article was submitted to Extreme Microbiology, substrates, while loose rocks contained a diverse microbial community, including a section of the journal Actinobacteria, Alphaproteobacteria and abundant Cyanobacteria inhabiting the milder and Frontiers in Microbiology diverse microhabitats within. Archaea, a domain never described before in similar Antarctic Received: 22 February 2021 environments, were also consistently found in the three substrates, but being more abundant Accepted: 21 May 2021 13 Published: 02 July2021 and potentially more active in soils. Stable isotopic ratios of total carbon (δ C) and nitrogen 15 Citation: (δ N), soluble anions concentrations, and the detection of proteins involved in key Fernández-Martínez MÁ, metabolisms via the Life Detector Chip (LDChip), suggest that microbial primary production García-Villadangos M, Moreno-Paz M, Gangloff V, Carrizo D, has a pivotal role in nutrient cycling at these exposed areas with limited deposition of Blanco Y, González S, nutrients. Detection of stress-resistance proteins, such as molecular chaperons, suggests Sánchez-García L, microbial molecular adaptation mechanisms to cope with these harsh conditions. Since Prieto-Ballesteros O, Altshuler I, Whyte LG, Parro V and early Mars may have encompassed analogous environmental conditions as the ones found Fairén AG (2021) Geomicrobiological in these Antarctic nunataks, our study also contributes to the understanding of the metabolic Heterogeneity of Lithic Habitats in the Extreme Environment of Antarctic features and biomarker profiles of a potential Martian microbiota, as well as the use of Nunataks: A Potential Early LDChip in future life detection missions. Mars Analog. Front. Microbiol. 12:670982. Keywords: polar microbiology, nunatak, environmental microbiology, terrestrial analogs of Martian habitats, doi: 10.3389/fmicb.2021.670982 astrobiology Frontiers in Microbiology | www.frontiersin.org 1 July 2021 | Volume 12 | Article 670982 Fernández-Martínez et al. Geomicrobiology of Antarctic Nunataks INTRODUCTION (Cary et al., 2010; Lambrechts et al., 2019; Garrido-Benavent et al., 2020). The Archaea domain has been much less studied Only a small area on Antarctica is permanently ice-free, in these ecosystems, showing a restricted distribution and lower corresponding to approximately 49,500 km2 (0.35–0.40% of concentration of cells, with no members isolated from soil total surface (Bockheim et al., 2015; Convey et al., 2018). Half ice-free areas other than geothermally heated ones (Niederberger of these ice-free 49,500 km2 correspond to the Transantarctic et al., 2012; Amenábar et al., 2013; Bendia et al., 2018; Lambrechts Mountains, while other 20% are located along the Antarctic et al., 2019). Described Antarctic soil archaeal communities Peninsula region (Bockheim et al., 2015). Exposed terrains in mainly included members within Euryarchaeota, Thaumarchaeota most of the Antarctic ice-free regions mainly consist of sandy and Crenarchaeota phyla (Bates et al., 2011; Richter et al., material with very low organic matter and microbial populations 2014; Pessi et al., 2015; Zhang et al., 2020). (Lambrechts et al., 2019). Therefore, they can be considered Several Antarctic microbial taxa have developed strategies representatives of one of four different orders of soil, i.e. Gelisols, to colonize rocks as their primary niche (i.e., ‘lithobionts’), Entisols, Inceptisols and Histosols (Cowan et al., 2014; Bockheim following an avoidance strategy since rocks harbor a more et al., 2015; Garrido-Benavent et al., 2020). Particular formations stable environment inside (De Los Ríos et al., 2014; Yung within these exposed areas are the peaks from a mountain et al., 2014; Coleine et al., 2020). Endolithic microorganisms range that protrude above a surrounding ice cap or glacier, can thus colonize different spaces within rocks: chasmoendoliths also known as nunataks (from Inuit nunataq, lonely peak). appear on cracks and fissures in contrast to cryptoendoliths, Nunataks usually present a small alteration of soils that even which grow on pores formed after weathering of rocks Pointing( allows bedrock to be studied. Thus, they represent unique, et al., 2009; Cowan, 2014; De Los Ríos et al., 2014; Archer mostly pristine environments that can be considered as ideal et al., 2016). This endolithic community establishment requires natural laboratories for polar studies. Although nunataks can the formation of complex biofilms within the cracks and pores be found in continental and peninsular (including archipelagos and sometimes lead to a layered pattern of colonization, following close to it) regions of Antarctica, they have received little location of radiation-protecting pigments or even different attention from a biological perspective, with only a few studies microbial communities (Friedmann, 1982; Pointing and Belnap, analysing nunatak microbiology in the last decades [e.g., 2012; De Los Ríos et al., 2014; Yung et al., 2014; Archer et al., (Brinkmann et al., 2007; Yergeau et al., 2009), both studying 2016; Crits-Christoph et al., 2016; Wierzchos et al., 2018). Coal Nunatak in Alexander Island, 72°03' S 68°31' W, and Specifically, rocks offer a shelter against surrounding climatic (Almela et al., 2021), not focused but including samples from harshness and UV radiation, acting as a reservoir of water Clark Nunatak, Byers Peninsula, Livingston Island]. and a warmer environment (up to 5–15°C above air temperature Within lithic environments, soils are characterized by having in specific thermal flux areas). However, rocks, and especially an enormous heterogeneity in geochemical parameters that bedrock, are highly oligotrophic environments (Kirby et al., leads to niche partitioning, including variations in vertical 2012; Amarelle et al., 2019). Consequently, it has been suggested profiles in the scale of a few centimeters Cary( et al., 2010; that the principal carbon and nitrogen inputs for nutrient Bottos et al., 2014; Bockheim et al., 2015; Almela et al., 2021). cycling in endolithic environments come from photoautotrophic Consequently, these ecosystems usually contain high microbial and diazotrophic microorganisms (Cowan et al., 2014; Amarelle diversity – discoveries of novel lineages are frequent – with et al., 2019; Garrido-Benavent et al., 2020). Hence, lithobiontic reduced space for the different populations to develop, and a communities in Antarctica are primarily composed of the higher influence of stochastic events on the inhabiting Cyanobacteria and Proteobacteria phyla, but with a high incidence communities (Bottos et al., 2014; Feeser et al., 2018). To date, of fungi and lichens (de la Torre et al., 2003; Cary et al., microbial communities from exposed Antarctic soils have 2010; De Los Ríos et al., 2014; Benavent-González et al., 2018; received moderate attention, despite their importance to Amarelle et al., 2019; Garrido-Benavent et al., 2020), while ecosystem function (Cary et al., 2010; Bottos et al., 2014; Archaea have been recently described as absent from rock- Niederberger et al., 2015; Feeser et al., 2018; Lambrechts et al., inhabiting communities in such extreme environments (Crits- 2019; Garrido-Benavent et al., 2020; Almela et al., 2021). These Christoph et al., 2016). While many studies employed microscopy microbial communities are mainly composed of psychrotolerant to describe Antarctic microbial lithic communities [reviewed organisms, with
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