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      Altiarchaeales”: Uncultivated Archaea from the Subsurface

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          Abstract

          Due to the limited cultivability of the vast majority of microorganisms, researchers have applied environmental genomics and other state-of-the-art technologies to gain insights into the biology of uncultivated Archaea and bacteria in their natural biotope. In this review, we summarize the scientific findings on a recently proposed order-level lineage of uncultivated Archaea called Altiarchaeales, which includes “ Candidatus Altiarchaeum hamiconexum” as the most well-described representative. Ca. A. hamiconexum possesses a complex biology: thriving strictly anaerobically, this microorganism is capable of forming highly-pure biofilms, connecting the cells by extraordinary cell surface appendages (the “hami”) and has other highly unusual traits, such as a double-membrane-based cell wall. Indicated by genomic information from different biotopes, the Altiarchaeales seem to proliferate in deep, anoxic groundwater of Earth’s crust bearing a potentially very important function: carbon fixation. Although their net carbon fixation rate has not yet been determined, they appear as highly abundant organisms in their biotopes and may thus represent an important primary producer in the subsurface. In sum, the research over more than a decade on Ca. A. hamiconexum has revealed many interesting features of its lifestyle, its genomic information, metabolism and ultrastructure, making this archaeon one of the best-studied uncultivated Archaea in the literature.

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          Most cited references34

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          CRISPR--a widespread system that provides acquired resistance against phages in bacteria and archaea.

          Arrays of clustered, regularly interspaced short palindromic repeats (CRISPRs) are widespread in the genomes of many bacteria and almost all archaea. These arrays are composed of direct repeats that are separated by similarly sized non-repetitive spacers. CRISPR arrays, together with a group of associated proteins, confer resistance to phages, possibly by an RNA-interference-like mechanism. This Progress discusses the structure and function of this newly recognized antiviral mechanism.
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            Adaptations to energy stress dictate the ecology and evolution of the Archaea.

            The three domains of life on Earth include the two prokaryotic groups, Archaea and Bacteria. The Archaea are distinguished from Bacteriabased on phylogenetic and biochemical differences, but currently there is no unifying ecological principle to differentiate these groups. The ecology of the Archaea is reviewed here in terms of cellular bioenergetics. Adaptation to chronic energy stress is hypothesized to be the crucial factor that distinguishes the Archaea from Bacteria. The biochemical mechanisms that enable archaea to cope with chronic energy stress include low-permeability membranes and specific catabolic pathways. Based on the ecological unity and biochemical adaptations among archaea, I propose the hypothesis that chronic energy stress is the primary selective pressure governing the evolution of the Archaea.
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              Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces.

              During attempts to obtain novel, human-associated species of the domain Archaea, a coccoid micro-organism, designated strain B10(T), was isolated in pure culture from a sample of human faeces collected in Marseille, France. On the basis of its phenotypic characteristics and 16S rRNA and mcrA gene sequences, the novel strain was classified as a methanogenic archaeon. Cells of the strain were non-motile, Gram-staining-positive cocci that were approximately 850 nm in diameter and showed autofluorescence at 420 nm. Cells were lysed by 0.1% (w/v) SDS. With hydrogen as the electron donor, strain B10(T) produced methane by reducing methanol. The novel strain was unable to produce methane when hydrogen or methanol was the sole energy source. In an atmosphere containing CO(2), strain B10(T) could not produce methane from formate, acetate, trimethylamine, 2-butanol, 2-propanol, cyclopentanol, 2-pentanol, ethanol, 1-propanol or 2,3-butanediol. Strain B10(T) grew optimally with 0.5-1.0% (w/v) NaCl, at pH 7.6 and at 37 °C. It required tungstate-selenite for growth. The complete genome of the novel strain was sequenced; the size of the genome was estimated to be 2.05 Mb and the genomic DNA G+C content was 59.93 mol%. In phylogenetic analyses based on 16S rRNA gene sequences, the highest sequence similarities (98.0-98.7%) were seen between strain B10(T) and several uncultured, methanogenic Archaea that had been collected from the digestive tracts of a cockroach, a chicken and mammals. In the same analysis, the non-methanogenic 'Candidatus Aciduliprofundum boonei' DSM 19572 was identified as the cultured micro-organism that was most closely related to strain B10(T) (83.0% 16S rRNA gene sequence similarity). Each of the three treeing algorithms used in the analysis of 16S rRNA gene sequences indicated that strain B10(T) belongs to a novel order that is distinct from the Thermoplasmatales. The novel strain also appeared to be distinct from Methanosphaera stadtmanae DSM 3091(T) (72.9% 16S rRNA gene sequence similarity), another methanogenic archaeon that was isolated from human faeces and can use methanol in the presence of hydrogen. Based on the genetic and phenotypic evidence, strain B10(T) represents a novel species of a new genus for which the name Methanomassiliicoccus luminyensis gen. nov., sp. nov. is proposed. The type strain of the type species is B10(T) ( = DSM 24529(T) = CSUR P135(T)).
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                Author and article information

                Contributors
                Role: Academic Editor
                Role: Academic Editor
                Role: Academic Editor
                Journal
                Life (Basel)
                Life (Basel)
                life
                Life
                MDPI
                2075-1729
                12 May 2015
                June 2015
                : 5
                : 2
                : 1381-1395
                Affiliations
                [1 ]Department of Earth and Planetary Science, University of California, Berkeley, 307 McCone Hall, Berkeley, CA 94720, USA; E-Mail: alexander.j.probst@ 123456gmail.com
                [2 ]Interactive Microbiome Research, Section of Infectious Diseases and Tropical Medicine, Department of Internal Medicine, Medical University Graz, Graz 8036, Austria
                [3 ]BioTechMed, Krenngasse 37, Graz 8010, Austria
                Author notes
                [* ]Author to whom correspondence should be addressed; E-Mail: christine.moissl-eichinger@ 123456medunigraz.at ; Tel.: +43-316-385-72808.
                Article
                life-05-01381
                10.3390/life5021381
                4500143
                25984733
                7d0bb427-0032-4cc6-911b-c4ce295f13a5
                © 2015 by the authors; licensee MDPI, Basel, Switzerland.

                This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 March 2015
                : 05 May 2015
                Categories
                Review

                archaea,subsurface,uncultivated,hami,sulfidic springs
                archaea, subsurface, uncultivated, hami, sulfidic springs

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