Lineages of Acidophilic Archaea Revealed by Community Genomic Analysis

Department of Earth and Planetary Sciences, University of California, Berkeley, CA 94720, USA.
Science (Impact Factor: 33.61). 12/2006; 314(5807):1933-5. DOI: 10.1126/science.1132690
Source: PubMed


Novel, low-abundance microbial species can be easily overlooked in standard polymerase chain reaction (PCR)-based surveys. We used community genomic data obtained without PCR or cultivation to reconstruct DNA fragments bearing unusual 16S ribosomal RNA (rRNA) and protein-coding genes from organisms belonging to novel archaeal lineages. The organisms are minor components of all biofilms growing in pH 0.5 to 1.5 solutions within the Richmond Mine, California. Probes specific for 16S rRNA showed that the fraction less than 0.45 micrometers in diameter is dominated by these organisms. Transmission electron microscope images revealed that the cells are pleomorphic with unusual folded membrane protrusions and have apparent volumes of <0.006 cubic micrometer.

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    • "Two decades of 16S rRNA gene-based molecular surveys have revealed the microbial diversity and ecology of AMD environments (Goebel and Stackebrandt, 1994; Baker and Banfield, 2003; Johnson and Hallberg, 2003; Amaral-Zettler et al., 2011; Kuang et al., 2012). More recently, metagenomic analyses have successfully reconstructed complete or near-complete genomes of dominant AMD microbes directly from environmental samples, possible scenarios for carbon and nitrogen fixation and energy generation, and their potential roles in acid generation have been suggested (Tyson et al., 2004; Baker et al., 2006). On the basis of metagenome-derived genomic information, subsequent metaproteomics have revealed the occurrence of proteins associated with the generation of AMD and the adaptation to extremely acidic habitats (Ram et al., 2005; Baker et al., 2010; Bertin et al., 2011; Méndez-García et al., 2014). "
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    ABSTRACT: The microbial communities in acid mine drainage have been extensively studied to reveal their roles in acid generation and adaption to this environment. Lacking, however, are integrated community- and organism-wide comparative gene transcriptional analyses that could reveal the response and adaptation mechanisms of these extraordinary microorganisms to different environmental conditions. In this study, comparative metagenomics and metatranscriptomics were performed on microbial assemblages collected from four geochemically distinct acid mine drainage (AMD) sites. Taxonomic analysis uncovered unexpectedly high microbial biodiversity of these extremely acidophilic communities, and the abundant taxa of Acidithiobacillus, Leptospirillum and Acidiphilium exhibited high transcriptional activities. Community-wide comparative analyses clearly showed that the AMD microorganisms adapted to the different environmental conditions via regulating the expression of genes involved in multiple in situ functional activities, including low-pH adaptation, carbon, nitrogen and phosphate assimilation, energy generation, environmental stress resistance, and other functions. Organism-wide comparative analyses of the active taxa revealed environment-dependent gene transcriptional profiles, especially the distinct strategies used by Acidithiobacillus ferrivorans and Leptospirillum ferrodiazotrophum in nutrients assimilation and energy generation for survival under different conditions. Overall, these findings demonstrate that the gene transcriptional profiles of AMD microorganisms are closely related to the site physiochemical characteristics, providing clues into the microbial response and adaptation mechanisms in the oligotrophic, extremely acidic environments.The ISME Journal advance online publication, 23 December 2014; doi:10.1038/ismej.2014.245.
    Full-text · Article · Dec 2014 · The ISME Journal
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    • "Metagenomics has previously been used to reconstruct microbial genomic potential and to predict microbial structure from diverse environments [8-12]. Many metagenomic studies involved the reconstruction of single organisms (or species-level populations), linking metabolic functions with phylogeny [8,13,14]. Expanding our understanding of the genomic content of species from the environment is crucial in determining the putative roles these organisms play within in the ecosystem. However, extrapolating 16S rRNA gene sequence similarity to putative functional roles is confounded due to large genomic variations in between related organisms, with as much as 60% dissimilarity in gene content [15,16]. "
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    ABSTRACT: Background The Gulf of Maine is an important biological province of the Northwest Atlantic with high productivity year round. From an environmental Sanger-based metagenome, sampled in summer and winter, we were able to assemble and explore the partial environmental genomes of uncultured members of the class Flavobacteria. Each of the environmental genomes represents organisms that compose less than 1% of the total microbial metagenome. Results Four partial environmental genomes were assembled with varying degrees of estimated completeness (37%?84% complete) and were analyzed from a perspective of gathering information regarding niche partitioning between co-occurring organisms. Comparative genomics revealed potentially important niche partitioning genomic variations, including iron transporters and genes associated with cell attachment and polymer degradation. Analysis of large syntenic regions helped reveal potentially ecologically relevant variations for Flavobacteriaceae in the Gulf of Maine, such as arginine biosynthesis, and identify a putative genomic island incorporating novel exogenous genes from the environment. Conclusions Biogeographic analysis revealed flavobacteria species with distinct abundance patterns suggesting the presence of local blooms relative to the other species, as well as seasonally selected organisms. The analysis of genomic content for the Gulf of Maine Flavobacteria supports the hypothesis of a particle-associated lifestyle and specifically highlights a number of putative coding sequences that may play a role in the remineralization of particulate organic matter. And lastly, analysis of the underlying sequences for each assembled genome revealed seasonal and nonseasonal variants of specific genes implicating a dynamic interaction between individuals within the species.
    Full-text · Article · Sep 2014
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    • "The AMD microbial community samples contain Thermoplasmatales lineage archaea referred to as Aplasma, Eplasma, Gplasma, Ferroplasmas Fer1 and Fer2 [related to previously described Ferroplasma and Thermoplasma acidophilum (Golyshina and Timmis, 2005)]; Iplasma from a sibling lineage to the Thermoplasmatales (Yelton et al., 2013); as well as ARMAN nanoarchaea (Baker et al., 2006). Whole ultrastructural characterization of ARMAN nanoarchaea was reported previously (Comolli et al., 2009); their cell walls are smooth and uniform in thickness (~30 ± 2 nm wide), with conspicuous inner and outer membranes (IM, OM) and no S-layer. "
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    ABSTRACT: Metagenomic studies are revolutionizing our understanding of microbes in the biosphere. They have uncovered numerous proteins of unknown function in tens of essentially unstudied lineages that lack cultivated representatives. Notably, few of these microorganisms have been visualized, and even fewer have been described ultra-structurally in their essentially intact, physiologically relevant states. Here, we present cryogenic transmission electron microscope (cryo-TEM) 2D images and 3D tomographic datasets for archaeal species from natural acid mine drainage (AMD) microbial communities. Ultrastructural findings indicate the importance of microbial interconnectedness via a range of mechanisms, including direct cytoplasmic bridges and pervasive pili. The data also suggest a variety of biological structures associated with cell-cell interfaces that lack explanation. Some may play roles in inter-species interactions. Interdependences amongst the archaea may have confounded prior isolation efforts. Overall, the findings underline knowledge gaps related to archaeal cell components and highlight the likely importance of co-evolution in shaping microbial lineages.
    Full-text · Article · Jul 2014 · Frontiers in Microbiology
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