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.