A Mosaic of Geothermal and Marine Features Shapes Microbial Community Structure on Deception Island Volcano, Antarctica

Abstract

Active volcanoes in Antarctica contrast with their predominantly cold surroundings, resulting in environmental conditions capable of selecting for versatile and extremely diverse microbial communities. This is especially true on Deception Island, where geothermal, marine, and polar environments combine to create an extraordinary range of environmental conditions. Our main goal in this study was to understand how microbial community structure is shaped by gradients of temperature, salinity, and geochemistry in polar marine volcanoes. Thereby, we collected surface sediment samples associated with fumaroles and glaciers at two sites on Deception, with temperatures ranging from 0 to 98°C. Sequencing of the 16S rRNA gene was performed to assess the composition and diversity of Bacteria and Archaea. Our results revealed that Deception harbors a combination of taxonomic groups commonly found both in cold and geothermal environments of continental Antarctica, and also groups normally identified at deep and shallow-sea hydrothermal vents, such as hyperthermophilic archaea. We observed a clear separation in microbial community structure across environmental gradients, suggesting that microbial community structure is strongly niche driven on Deception. Bacterial community structure was significantly associated with temperature, pH, salinity, and chemical composition; in contrast, archaeal community structure was strongly associated only with temperature. Our work suggests that Deception represents a peculiar “open-air” laboratory to elucidate central questions regarding molecular adaptability, microbial evolution, and biogeography of extremophiles in polar regions.

Surviving in hot and cold: psychrophiles and thermophiles from Deception Island volcano, Antarctica

“…Indeed, in a previous work, we detected only archaeal 16S rRNA sequences in FBA sample using Illumina sequencing technique (Bendia et al, 2018 …”

“…Carrión et al (2011) isolated eight strains of marine sediments from the island, belonging to the genera Pseudomonas, Marinobacter, and Shewanella, and one of these strains was classified as a new species, proposed Pseudomonas deceptionensis. In a previous work, we reported the presence of several extremophiles-related sequences (psychrophiles, thermophiles, hyperthermophiles, and halophiles) among extreme temperature gradients in Deception (Bendia et al 2018). However, since only 16S rRNA gene sequences were evaluated, it was not possible to know if these extremophiles were viable in those conditions.…”

Metabolic potential and survival strategies of microbial communities across extreme temperature gradients on Deception Island volcano, Antarctica

“…The majority of these previous studies have focused on nonpolar thermal ecosystems, where the temperature range is narrower than in polar volcanoes; the exception is a study of deep-sea hydrothermal vents, in which the contrasting temperatures are created by the contact of heat with the surrounding cold seawater (with temperatures 0-4 o C). Indeed, the Deception communities from fumaroles have similar members (Bendia et al, 2018b) 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.…”

“…To compare our results with the study performed by Bendia et al (2018b), we used the same dataset and DNA extractions as a template for the metagenomics. Due to low DNA mass even after several concentration efforts, extracted DNA was subjected to multiple displacement amplification (MDA) using the illustra GenomiPhi V2 DNA amplification kit (GE Healthcare, Piscataway, NJ, USA), following the manufacturer's instructions.…”

“…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 et al, 2018b), 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 as Pyrodictium spp.…”