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

Abstract

Active volcanoes in Antarctica have remarkable temperature and geochemical gradients that could select for a wide variety of microbial adaptive mechanisms and metabolic pathways. Deception Island is a stratovolcano flooded by the sea, resulting in contrasting ecosystems such as permanent glaciers and active fumaroles, which creates steep gradients that have been shown to affect microbial diversity. In this study, we used shotgun metagenomics and metagenome-assembled genomes to explore the metabolic potentials and survival strategies of microbial communities along an extreme temperature gradient in fumarole and glacier sediments on Deception Island. We observed that communities from a 98 C fumarole were significantly enriched in genes related to hyperthermophilic (e.g. reverse gyrase, GroEL/GroES and thermosome) and oxidative stress responses, as well as genes related to sulfate reduction, ammonification and carbon fixation. Communities from <80 C fumaroles possessed more genes related osmotic, cold-and heat-shock responses, and diverse metabolic potentials, such as those related to sulfur oxidation and denitrification, while glacier communities showed abundant metabolic potentials mainly related to heterotrophy. Through the reconstruction of genomes, we were able to reveal the metabolic potentials and different survival strategies of underrepresented taxonomic groups, especially those related to Nanoarchaeota, Pyrodictiaceae and thermophilic ammonia-oxidizing archaeal lineages.

Islands Within Islands: Bacterial Phylogenetic Structure and Consortia in Hawaiian Lava Caves and Fumaroles

“…Network analyses concluded that the overall complexity of interactions among bacteria is higher in geothermal environments than in lava caves. Bendia et al ( 2021 ) reported a similar pattern of greater complexity in microbial communities along a thermal gradient. This observation may reflect the more extreme nature of the environment and lower diversity overall, a situation in which more synergistic metabolic interactions may be required for survival, with fewer individual strains or species able to fulfill the required ecological roles (greater number of hubs).…”

Polyphasic Analysis Reveals Potential Petroleum Hydrocarbon Degradation and Biosurfactant Production by Rare Biosphere Thermophilic Bacteria From Deception Island, an Active Antarctic Volcano

“…The DNA used to perform the metagenomic sequencing was extracted from samples collected in the same area where the samples for isolating bacteria were obtained. The DNA extraction and metagenome sequencing (Shotgun) methods were described by Bendia et al (2021) . Reads were filtered using SICKLE software ( Joshi and Fass, 2011 ), using a minimum Phred score of 30.…”

“…Metagenomic approaches, in which the total DNA is extracted directly from environmental samples and shotgun-sequenced ( Kunin et al, 2008 ), have been used to investigate microbial communities and their functions in various extreme environments, such as thermal pools ( Wilkins et al, 2019 ), desert biological soil crusts ( Meier et al, 2021 ), permafrost ( Woodcroft et al, 2018 ), and Antarctic microbial mat and soil ( Zaikova et al, 2019 ; Bendia et al, 2021 ). Nearly complete genomes have been assembled from shotgun-sequenced metagenomes from these environments.…”

“…Despite the advent of omics analysis, culture studies are still important to assess the physiological properties of bacterial cells and to cover the limits of detection of independent-culture methods ( Zamkovaya et al, 2021 ). Such studies allow us to understand the survival strategies and metabolic adaptations of bacteria ( Bendia et al, 2021 ) and to explore their potential for use in different areas of biotechnology, through culturomics and deep genomic analyses ( Schultz and Rosado, 2019 , 2020 ).…”

Variation of Structure and Cellular Functions of Type IA Topoisomerases across the Tree of Life

“…Genetic studies suggested that the other reverse gyrase TopR2 in Sulfolobales may have another more important function [ 122 ]. Based on previous work, the requirement of reverse gyrase activity for hyperthermophiles [ 28 , 123 ] may be related to DNA protection and repair in addition to positive DNA supercoiling [ 29 , 124 , 125 ].…”