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

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          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.

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          Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol.

          The widespread occurrence and diversity of ammonia oxidizing Archaea suggests their contribution to the nitrogen cycle is of global significance. Their distribution appeared limited to low- and moderate-temperature environments until the recent finding of a diagnostic membrane lipid, crenarchaeol, in terrestrial hot springs. We report here the cultivation of a thermophilic nitrifier ('Candidatus Nitrosocaldus yellowstonii'), an autotrophic crenarchaeote growing up to 74 degrees C by aerobic ammonia oxidation. The major core lipid of this archaeon growing at 72 degrees C is crenarchaeol, providing the first direct evidence for its synthesis by a thermophile. These findings greatly extend the upper temperature limit of nitrification and document that the capacity for ammonia oxidation is broadly distributed among the Crenarchaeota.
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            Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia.

            Aerobic methanotrophic bacteria consume methane as it diffuses away from methanogenic zones of soil and sediment. They act as a biofilter to reduce methane emissions to the atmosphere, and they are therefore targets in strategies to combat global climate change. No cultured methanotroph grows optimally below pH 5, but some environments with active methane cycles are very acidic. Here we describe an extremely acidophilic methanotroph that grows optimally at pH 2.0-2.5. Unlike the known methanotrophs, it does not belong to the phylum Proteobacteria but rather to the Verrucomicrobia, a widespread and diverse bacterial phylum that primarily comprises uncultivated species with unknown genotypes. Analysis of its draft genome detected genes encoding particulate methane monooxygenase that were homologous to genes found in methanotrophic proteobacteria. However, known genetic modules for methanol and formaldehyde oxidation were incomplete or missing, suggesting that the bacterium uses some novel methylotrophic pathways. Phylogenetic analysis of its three pmoA genes (encoding a subunit of particulate methane monooxygenase) placed them into a distinct cluster from proteobacterial homologues. This indicates an ancient divergence of Verrucomicrobia and Proteobacteria methanotrophs rather than a recent horizontal gene transfer of methanotrophic ability. The findings show that methanotrophy in the Bacteria is more taxonomically, ecologically and genetically diverse than previously thought, and that previous studies have failed to assess the full diversity of methanotrophs in acidic environments.
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              The Complete Genome Sequence of Haloferax volcanii DS2, a Model Archaeon

              Background Haloferax volcanii is an easily culturable moderate halophile that grows on simple defined media, is readily transformable, and has a relatively stable genome. This, in combination with its biochemical and genetic tractability, has made Hfx. volcanii a key model organism, not only for the study of halophilicity, but also for archaeal biology in general. Methodology/Principal Findings We report here the sequencing and analysis of the genome of Hfx. volcanii DS2, the type strain of this species. The genome contains a main 2.848 Mb chromosome, three smaller chromosomes pHV1, 3, 4 (85, 438, 636 kb, respectively) and the pHV2 plasmid (6.4 kb). Conclusions/Significance The completed genome sequence, presented here, provides an invaluable tool for further in vivo and in vitro studies of Hfx. volcanii.
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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
                07 May 2018
                2018
                : 9
                : 899
                Affiliations
                [1] 1Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo , São Paulo, Brazil
                [2] 2Department of Biology, Institute of Ecology and Evolution, University of Oregon , Eugene, OR, United States
                Author notes

                Edited by: Alison Elizabeth Murray, Desert Research Institute, United States

                Reviewed by: William P. Inskeep, Montana State University, United States; Charles K. Lee, The University of Waikato, New Zealand

                *Correspondence: Vivian H. Pellizari, vivianp@ 123456usp.br

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

                Article
                10.3389/fmicb.2018.00899
                5949364
                1a0d0cb8-4e0a-428d-81ea-2195b4f89c5d
                Copyright © 2018 Bendia, Signori, Franco, Duarte, Bohannan and Pellizari.

                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 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
                : 24 November 2017
                : 18 April 2018
                Page count
                Figures: 7, Tables: 0, Equations: 0, References: 67, Pages: 13, Words: 0
                Funding
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico 10.13039/501100003593
                Award ID: 407816/2013-5
                Award ID: 028306/2009
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo 10.13039/501100001807
                Award ID: 2012/23241-0
                Award ID: 2012/11037-0
                Award ID: 2016/16183-5
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                polar marine volcano,antarctica,environmental gradients,extremophiles,diversity,community structure

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