Mechanisms of unique chaotropic resistance and biocalcification in a halophilic Virgibacillus isolated from ephemeral microbial mats of the calcium-rich Don Juan pond in Antarctica
8 affiliations
- 1Institute of Polar Sciences, ISP-CNR
- 2Orenburg Federal Research Center, Institute for Cellular and Intracellular Symbiosis, Ural Branch of RAS
- 3Department of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne
- 4ARC Centre for Cryo-electron Microscopy of Membrane Proteins, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne
- 5Institute for Marine Biological Resources and Biotechnology, IRBIM-CNR
- 6Eni Rewind EE&MD/SELAB
- 7Department of Biochemistry, Genetics and Microbiology, Centre for Bioinformatics and Computational Biology, University of Pretoria
- 8Winogradsky Institute of Microbiology, Research Centre of Biotechnology RAS
Abstract
Introduction: Don Juan Pond (DJP), located in the McMurdo Dry Valleys of Antarctica, is one of the most extreme cold aquatic environments on our planet and most similar to Mars due to its CaCl₂-rich brines, low water activity, exceptional chaotropicity, average annual subzero temperatures and intense solar radiation during the Antarctic summer. Although the central DJP brine is considered anathema to life, the surrounding basin seasonally hosts temporary streams, ponds, and, very rarely, ephemeral microbial mats.
Methods: In this study, we investigated the diversity of these microbial mats and attempted to cultivate Ca ²⁺ -tolerant bacteria and analyze the phenotypic and molecular characteristics of the most promising isolates. To understand the molecular mechanisms underlying their adaptive strategy, further analysis of their genomic potential, adaptive epigenetic transformations and differential transcriptomics was conducted. Predicted functions were verified through physiological experiments.
Results: The most calcium-tolerant isolate, Virgibacillus flavescens DJP025-4, was studied in detail, including its adaptive physiology and, in particular, its remarkable tolerance to varying calcium concentrations, unmatched by other prokaryotes. DJP025-4 cells were able to survive and remain cultivable after 3 months of exposure to 3.0 M Ca ²⁺ , corresponding to a water activity of approximately 0.63 and total chaotropicity value of +276.6 kJ kg ⁻¹ , conditions well below the current limit for life survival equivalent. Transcriptome analysis revealed that the primary metabolic response of strain DJP025-4 to Ca ²⁺ stress includes enzymatically induced urease-independent CaCO ₃ precipitation, enhanced uptake of external compatible solutes, and activation of cell surface structures biosynthesis, including peptidoglycan metabolism, biofilm matrix formation, and cellular appendage assembly, which finally increase the cell surface area and the number of Ca 2 + precipitation centers on it. Whole-genome analysis revealed a high degree of genetic plasticity in this bacterium, involving natural transformation with genetic material acquired from the bacterial community and adaptive epigenetic mechanisms of gene regulation.
Discussion: Among the key findings, it is worth noting that, in addition to developing remarkable adaptation mechanisms to withstand and thrive in a harsh, calcium-rich environment, strain DJP025-4 appears to remain dependent on the presence of external compatible solutes. We hypothesize that within the DJP stream ecosystem, it is able to survive at high Ca ²⁺ concentrations by utilizing trace amounts of such substances produced by other organisms, specifically, moderate halophiles inhabiting surface microbial mats in lower-salinity zones, which release dissolved organic matter and osmolytes into the environment.
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BibTeX
@article{marturano2026mechanisms,
title = {{Mechanisms of unique chaotropic resistance and biocalcification in a halophilic Virgibacillus isolated from ephemeral microbial mats of the calcium-rich Don Juan pond in Antarctica}},
author = {Laura Marturano and Violetta La Cono and Francesco Smedile and Gina La Spada and Francesca Crisafi and Elena A. Selivanova and Marina E. Ignatenko and Manasi Mudaliyar and Debnath Ghosal and Enzo Messina and Alfonso Modica and Oleg N. Reva and Sergey N. Gavrilov and Michail M. Yakimov},
journal = {Frontiers in Microbiology},
year = {2026},
month = oct,
doi = {10.3389/fmicb.2026.1980805},
url = {https://www.frontiersin.org/articles/10.3389/fmicb.2026.1980805/full},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Mechanisms of unique chaotropic resistance and biocalcification in a halophilic Virgibacillus isolated from ephemeral microbial mats of the calcium-rich Don Juan pond in Antarctica
AU - Laura Marturano
AU - Violetta La Cono
AU - Francesco Smedile
AU - Gina La Spada
AU - Francesca Crisafi
AU - Elena A. Selivanova
AU - Marina E. Ignatenko
AU - Manasi Mudaliyar
AU - Debnath Ghosal
AU - Enzo Messina
AU - Alfonso Modica
AU - Oleg N. Reva
AU - Sergey N. Gavrilov
AU - Michail M. Yakimov
PY - 2026
DA - 2026/10/28
JO - Frontiers in Microbiology
DO - 10.3389/fmicb.2026.1980805
UR - https://www.frontiersin.org/articles/10.3389/fmicb.2026.1980805/full
AB - Introduction: Don Juan Pond (DJP), located in the McMurdo Dry Valleys of Antarctica, is one of the most extreme cold aquatic environments on our planet and most similar to Mars due to its CaCl₂-rich brines, low water activity, exceptional chaotropicity, average annual subzero temperatures and intense solar radiation during the Antarctic summer. Although the central DJP brine is considered anathema to life, the surrounding basin seasonally hosts temporary streams, ponds, and, very rarely, ephemeral microbial mats. Methods: In this study, we investigated the diversity of these microbial mats and attempted to cultivate Ca ²⁺ -tolerant bacteria and analyze the phenotypic and molecular characteristics of the most promising isolates. To understand the molecular mechanisms underlying their adaptive strategy, further analysis of their genomic potential, adaptive epigenetic transformations and differential transcriptomics was conducted. Predicted functions were verified through physiological experiments. Results: The most calcium-tolerant isolate, Virgibacillus flavescens DJP025-4, was studied in detail, including its adaptive physiology and, in particular, its remarkable tolerance to varying calcium concentrations, unmatched by other prokaryotes. DJP025-4 cells were able to survive and remain cultivable after 3 months of exposure to 3.0 M Ca ²⁺ , corresponding to a water activity of approximately 0.63 and total chaotropicity value of +276.6 kJ kg ⁻¹ , conditions well below the current limit for life survival equivalent. Transcriptome analysis revealed that the primary metabolic response of strain DJP025-4 to Ca ²⁺ stress includes enzymatically induced urease-independent CaCO ₃ precipitation, enhanced uptake of external compatible solutes, and activation of cell surface structures biosynthesis, including peptidoglycan metabolism, biofilm matrix formation, and cellular appendage assembly, which finally increase the cell surface area and the number of Ca 2 + precipitation centers on it. Whole-genome analysis revealed a high degree of genetic plasticity in this bacterium, involving natural transformation with genetic material acquired from the bacterial community and adaptive epigenetic mechanisms of gene regulation. Discussion: Among the key findings, it is worth noting that, in addition to developing remarkable adaptation mechanisms to withstand and thrive in a harsh, calcium-rich environment, strain DJP025-4 appears to remain dependent on the presence of external compatible solutes. We hypothesize that within the DJP stream ecosystem, it is able to survive at high Ca ²⁺ concentrations by utilizing trace amounts of such substances produced by other organisms, specifically, moderate halophiles inhabiting surface microbial mats in lower-salinity zones, which release dissolved organic matter and osmolytes into the environment.
SN - 1664-302X
ER -