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      The archaeal class Halobacteria and astrobiology: Knowledge gaps and research opportunities

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          Abstract

          Water bodies on Mars and the icy moons of the outer solar system are now recognized as likely being associated with high levels of salt. Therefore, the study of high salinity environments and their inhabitants has become increasingly relevant for Astrobiology. Members of the archaeal class Halobacteria are the most successful microbial group living in hypersaline conditions and are recognized as key model organisms for exposure experiments. Despite this, data for the class is uneven across taxa and widely dispersed across the literature, which has made it difficult to properly assess the potential for species of Halobacteria to survive under the polyextreme conditions found beyond Earth. Here we provide an overview of published data on astrobiology-linked exposure experiments performed with members of the Halobacteria, identifying clear knowledge gaps and research opportunities.

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          Global mineralogical and aqueous mars history derived from OMEGA/Mars Express data.

          Global mineralogical mapping of Mars by the Observatoire pour la Mineralogie, l'Eau, les Glaces et l'Activité (OMEGA) instrument on the European Space Agency's Mars Express spacecraft provides new information on Mars' geological and climatic history. Phyllosilicates formed by aqueous alteration very early in the planet's history (the "phyllocian" era) are found in the oldest terrains; sulfates were formed in a second era (the "theiikian" era) in an acidic environment. Beginning about 3.5 billion years ago, the last era (the "siderikian") is dominated by the formation of anhydrous ferric oxides in a slow superficial weathering, without liquid water playing a major role across the planet.
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            Microbial life at high salt concentrations: phylogenetic and metabolic diversity

            Halophiles are found in all three domains of life. Within the Bacteria we know halophiles within the phyla Cyanobacteria, Proteobacteria, Firmicutes, Actinobacteria, Spirochaetes, and Bacteroidetes. Within the Archaea the most salt-requiring microorganisms are found in the class Halobacteria. Halobacterium and most of its relatives require over 100–150 g/l salt for growth and structural stability. Also within the order Methanococci we encounter halophilic species. Halophiles and non-halophilic relatives are often found together in the phylogenetic tree, and many genera, families and orders have representatives with greatly different salt requirement and tolerance. A few phylogenetically coherent groups consist of halophiles only: the order Halobacteriales, family Halobacteriaceae (Euryarchaeota) and the anaerobic fermentative bacteria of the order Halanaerobiales (Firmicutes). The family Halomonadaceae (Gammaproteobacteria) almost exclusively contains halophiles. Halophilic microorganisms use two strategies to balance their cytoplasm osmotically with their medium. The first involves accumulation of molar concentrations of KCl. This strategy requires adaptation of the intracellular enzymatic machinery, as proteins should maintain their proper conformation and activity at near-saturating salt concentrations. The proteome of such organisms is highly acidic, and most proteins denature when suspended in low salt. Such microorganisms generally cannot survive in low salt media. The second strategy is to exclude salt from the cytoplasm and to synthesize and/or accumulate organic 'compatible' solutes that do not interfere with enzymatic activity. Few adaptations of the cells' proteome are needed, and organisms using the 'organic-solutes-in strategy' often adapt to a surprisingly broad salt concentration range. Most halophilic Bacteria, but also the halophilic methanogenic Archaea use such organic solutes. A variety of such solutes are known, including glycine betaine, ectoine and other amino acid derivatives, sugars and sugar alcohols. The 'high-salt-in strategy' is not limited to the Halobacteriaceae. The Halanaerobiales (Firmicutes) also accumulate salt rather than organic solutes. A third, phylogenetically unrelated organism accumulates KCl: the red extremely halophilic Salinibacter (Bacteroidetes), recently isolated from saltern crystallizer brines. Analysis of its genome showed many points of resemblance with the Halobacteriaceae, probably resulting from extensive horizontal gene transfer. The case of Salinibacter shows that more unusual types of halophiles may be waiting to be discovered.
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              Genome sequence of Halobacterium species NRC-1.

              We report the complete sequence of an extreme halophile, Halobacterium sp. NRC-1, harboring a dynamic 2,571,010-bp genome containing 91 insertion sequences representing 12 families and organized into a large chromosome and 2 related minichromosomes. The Halobacterium NRC-1 genome codes for 2,630 predicted proteins, 36% of which are unrelated to any previously reported. Analysis of the genome sequence shows the presence of pathways for uptake and utilization of amino acids, active sodium-proton antiporter and potassium uptake systems, sophisticated photosensory and signal transduction pathways, and DNA replication, transcription, and translation systems resembling more complex eukaryotic organisms. Whole proteome comparisons show the definite archaeal nature of this halophile with additional similarities to the Gram-positive Bacillus subtilis and other bacteria. The ease of culturing Halobacterium and the availability of methods for its genetic manipulation in the laboratory, including construction of gene knockouts and replacements, indicate this halophile can serve as an excellent model system among the archaea.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                13 October 2022
                2022
                : 13
                : 1023625
                Affiliations
                [1] 1State Key Laboratory of Lunar and Planetary Sciences, Macau University of Science and Technology (MUST) , Taipa, Macau SAR, China
                [2] 2China National Space Administration (CNSA), Macau Center for Space Exploration and Science , Taipa, Macau SAR, China
                [3] 3School of Life Sciences, University of Essex , Colchester, United Kingdom
                [4] 4German Aerospace Center (DLR), Institute of Aerospace Medicine , Köln, Germany
                [5] 5State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources and Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Life Sciences, Sun Yat-sen University , Guangzhou, China
                Author notes

                Edited by: Mohammad Ali Amoozegar, University of Tehran, Iran

                Reviewed by: Ricardo Amils, Autonomous University of Madrid, Spain; Bonnie K. Baxter, Westminster College, United States

                *Correspondence: André Antunes, aglantunes@ 123456must.edu.mo

                This article was submitted to Extreme Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2022.1023625
                9608585
                36312929
                83abdb78-9686-4cf7-9390-17f63c194534
                Copyright © 2022 Wu, McGenity, Rettberg, Simões, Li and Antunes.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 20 August 2022
                : 07 September 2022
                Page count
                Figures: 0, Tables: 1, Equations: 0, References: 207, Pages: 13, Words: 11507
                Funding
                Funded by: Macau University of Science and Technology, doi 10.13039/501100015260;
                Funded by: Macau University of Science and Technology, doi 10.13039/501100015260;
                Funded by: Fundo para o Desenvolvimento das Ciências e da Tecnologia, doi 10.13039/501100006469;
                Categories
                Microbiology
                Perspective

                Microbiology & Virology
                astrobiology,archaea,halobacteria,extremophiles,mars,icy moons
                Microbiology & Virology
                astrobiology, archaea, halobacteria, extremophiles, mars, icy moons

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