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.
Highlights
The fact that microbes shape the biosphere is well appreciated, but there are many blind spots in our understanding of the relevant processes because over half of all microbial phyla lack even a single characterized member (Baker and Dick, 2013)
Distinguishing Thermoplasmatales lineage archaea from the other archaea is straightforward on the basis of size and irregular and pleomorphic morphology and absence of cell wall (Yasuda et al, 1995; Golyshina and Timmis, 2005; Yelton et al, 2013 and references therein; Figures S2–S6)
Thermoplasmatales lineage archaea cells are generally bounded by a single membrane; all of the acid mine drainage (AMD) plasma genomes have putative Slayer genes, and genes potentially involved in archaeal S-layer protein N-glycosylation (Figures 2, 3; Figures S2–S6; Movies 1, 2; Yelton et al, 2013)
Summary
The fact that microbes shape the biosphere is well appreciated, but there are many blind spots in our understanding of the relevant processes because over half of all microbial phyla lack even a single characterized member (Baker and Dick, 2013). The approach can yield near-complete and even complete genomes (Albertsen et al, 2013; Sharon et al, 2013; references therein) These genomes provide a context for functional information from cultivationindependent transcriptomic, proteomic, or metabolomic measurements. In some cases ∼50% of proteins in organisms from lineages lacking cultivated representatives have no functional prediction (e.g., Kantor et al, 2013) Some of these proteins may be components of biochemically unknown ultrafine structures so far undetected in cultivated microorganisms or isolated organisms. Detection of such features by imaging methods provides a starting point for subsequent targeted investigations to uncover new structural features, appendages, or organelles. Even for structures that can be predicted (e.g., pili and flagella), imaging methods provide information that cannot be deduced from sequence information or expression assays (e.g., the distribution in cells or on cell surfaces, and certain structural characteristics)
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