Introduction
The study of life in extreme environments has long fascinated biologists. Understanding how life persists at environmental extremes provides insight into how living systems function, as well as providing a unique window into the evolutionary history of life itself (Merino et al., 2019). The Deception Island volcano contains a unique combination of extreme temperatures and geochemical energy sources that together have the potential for selecting a wide variety of microbial adaptive mechanisms and metabolic pathways. Deception Island is located in the South Shetland Islands at the spreading center of the Bransfield Strait marginal basin, which harbors contrasting ecosystems of permanent glaciers and active fumaroles with continuous emissions of gases, mostly carbon dioxide and hydrogen sulfide (Somoza et al., 2004). This combination of glaciers and fumaroles is produced by the interaction between the cryosphere and water mass contact with hot ascending magmas (Geyer et al., 2019). Unlike Antarctic continental volcanoes, Deception Island fumaroles reach up to 100 oC and have direct marine influence, creating a remarkable combination of thermal, geochemical and salinity gradients (Bartolini et al., 2014; Herbold et al., 2014; Muñoz-Martín et al., 2005).
While early research carried out on Deception focused primarily on obtaining bacterial isolates from hot or cold ecosystems (e.g. Carrión et al., 2011; Llarch et al., 1997; Stanley et al., 1967), a more recent study was able to recover both psychrophilic and thermophilic isolates among the steep temperature gradients (Bendia, Araujo, et al., 2018). Previous molecular studies described microbial diversity on Deception fumaroles using DGGE (Amenábar et al., 2013; Muñoz et al., 2011) and shotgun metagenomics to characterize the resistome profiles in cold sediments from Whalers Bay (Centurion et al., 2019). These previous studies were limited with respect to sampling depth and extent since only fumaroles or cold sediments were analyzed.
Two previous studies have focused on understanding the effect of Deception temperature gradients on microbial communities. The first, performed by our group, focused on determining taxonomic diversity through 16S rRNA gene sequencing (Bendia, Signori, et al., 2018), and a second study applied the Life Detector Chip (LDChip) to describe general functions of communities from Cerro Caliente (Lezcano et al., 2019). Our previous study showed that the steep gradients on Deception were able to select a unique combination of taxonomic groups found in deep and shallow hydrothermal vents (including hyperthermophilic Archaea, such asPyrodictium spp. ), geothermal systems and those typical from polar ecosystems (Bendia, Signori, et al., 2018). Also we reported that the bacterial community structure on Deception Island is strongly niche driven by a variety of environmental parameters (temperature, pH, salinity and volcanic geochemicals, such as sulfate), while archaeal diversity is mainly shaped by temperature (Bendia, Signori, et al., 2018). These previous studies, however, did not address the linkages between microbial structure and their adaptive and metabolic strategies over the particular environmental gradients found on Deception Island.
Although several studies have demonstrated that temperature is a primary driver of microbial taxonomic diversity in different geothermal and hydrothermal ecosystems (e.g. Antranikian et al., 2017; Price and Giovannelli, 2017; Sharp et al., 2014; Ward et al., 2017), it is still unclear to what extent temperature affects the functional processes of a microbial community, such as their adaptive mechanisms and metabolic pathways. The majority of these previous studies have focused on nonpolar thermal ecosystems, where the temperature range is not too broad as in polar volcanoes, with the exception of the deep-sea hydrothermal vents, in which the contrasting temperatures are created by the contact of heat with the surrounding cold seawater (temperature around 0-4 oC). Indeed, the Deception communities from fumaroles have similar members (Bendia, Signori, et al., 2018) to those found in deep-sea hydrothermal vents (e.g. Dick, 2019; Nakagawa et al., 2006; Takai et al., 2001), which suggests that, regarding differences in pressure (and other environmental effects), the wide temperature range typical of polar volcanoes and deep-sea hydrothermal vents can act as a strong selective pressure that favors (hyper)thermophilic specialists capable of thriving in high temperatures but that can also tolerate the cold surroundings.
Furthermore, there is controversy about the impact of extreme environments on microbe-microbe interactions. Although some studies have reported a decrease in the frequency of microbe-microbe interactions inferred from co-occurrence patterns (Cole et al., 2013; Merino et al., 2019; Sharp et al., 2014), others have observed the opposite trend (Lin et al., 2016; Mandakovic et al., 2018). The analysis of co-occurrence patterns is useful for examining the nature of the ecological rearrangements that take place in a microbial community facing contrasting environments (Freilich et al., 2010; Mandakovic et al., 2018).
In the current study, we assessed the microbial functional profile in fumarole and glacier sediments from two geothermal sites on the Deception Island volcano, Antarctica. For this, we performed shotgun metagenomics to unveil functional diversity and reconstructed genomes to reveal the microbes‘ putative lifestyles and survival capabilities, combining the genomic information with community functional profiles. Here, we hypothesize that (i) similar to what has been reported for community diversity, survival and metabolic strategies are also influenced by the combination of geochemical, salinity and extreme temperature gradients; (ii) these communities follow the redundancy of metabolic potential that was reported for deep-sea hydrothermal vent communities; and (iii) microbe-microbe interactions decrease with increasing temperature. This study adds important information regarding the ecological processes of microbial communities inhabiting a steep gradient of temperature, and addresses central questions regarding the functional adaptability of extremophiles in polar regions.