Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA

School of Chemistry and Molecular Biosciences, Australian Research Council Centre of Excellence for Integrative Legume Research, University of Queensland, St. Lucia, Queensland 4072, Australia.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 07/2010; 107(29):12883-8. DOI: 10.1073/pnas.1001085107
Source: PubMed


Endocytosis is a process by which extracellular material such as macromolecules can be incorporated into cells via a membrane-trafficking system. Although universal among eukaryotes, endocytosis has not been identified in Bacteria or Archaea. However, intracellular membranes are known to compartmentalize cells of bacteria in the phylum Planctomycetes, suggesting the potential for endocytosis and membrane trafficking in members of this phylum. Here we show that cells of the planctomycete Gemmata obscuriglobus have the ability to uptake proteins present in the external milieu in an energy-dependent process analogous to eukaryotic endocytosis, and that internalized proteins are associated with vesicle membranes. Occurrence of such ability in a bacterium is consistent with autogenous evolution of endocytosis and the endomembrane system in an ancestral noneukaryote cell.

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    • "Prokaryotes made many a start. There are examples of bacteria or archaea with nucleus-like structures (Lindsay et al. 2001), recombination (Smith et al. 1993), linear chromosomes (Bentley et al. 2002), internal membranes (Pinevich 1997), multiple replicons (Robinson and Bell 2007), giant size (Schulz and Jorgensen 2001), extreme polyploidy (Mendell et al. 2008), a dynamic cytoskeleton (Vats and Rothfield 2009), predation (Davidov and Jurkevitch 2009), parasitism (Moran 2007), introns and exons (Simon and Zimmerly 2008), intercellular signaling (Waters and Bassler 2005), endocytosis-like processes (Lonhienne et al. 2010), and even endosymbionts (Wujek 1979; von Dohlen et al. 2001). Yet, for each of these traits, bacteria and archaea stopped well short of the baroque complexity of eukaryotes. "
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    ABSTRACT: All morphologically complex life on Earth, beyond the level of cyanobacteria, is eukaryotic. All eukaryotes share a common ancestor that was already a complex cell. Despite their biochemical virtuosity, prokaryotes show little tendency to evolve eukaryotic traits or large genomes. Here I argue that prokaryotes are constrained by their membrane bioenergetics, for fundamental reasons relating to the origin of life. Eukaryotes arose in a rare endosymbiosis between two prokaryotes, which broke the energetic constraints on prokaryotes and gave rise to mitochondria. Loss of almost all mitochondrial genes produced an extreme genomic asymmetry, in which tiny mitochondrial genomes support, energetically, a massive nuclear genome, giving eukaryotes three to five orders of magnitude more energy per gene than prokaryotes. The requirement for endosymbiosis radically altered selection on eukaryotes, potentially explaining the evolution of unique traits, including the nucleus, sex, two sexes, speciation, and aging.
    Full-text · Article · May 2014 · Cold Spring Harbor perspectives in biology
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    • "After inoculation by streaking with sterile plastic loop charged with G. obscuriglobus grown on the same M1 agar medium, plates were sealed with parafilm before aerobic incubation. After 3 or 10 days of incubation, the cells were collected into an eppendorf tube containing 100 µl of Milli-Q deionized water and examined under phase contrast microscope to check the motility of the cells. 1 µg of GFP was added to the cells, mixed and incubated for 30 min at room temperature, then the cells were examined under fluorescence microscopy (confocal laser scanning) to assess their ability for uptake, as described elsewhere [34]. These standardized methods for medium preparation and culture incubation for 3–10 days were critical for optimal demonstration of GFP uptake [34]. "
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    ABSTRACT: Members of phylum Planctomycetes have been proposed to possess atypical cell organisation for the Bacteria, having a structure of sectioned cells consistent with internal compartments surrounded by membranes. Here via electron tomography we confirm the presence of compartments in the planctomycete Gemmata obscuriglobus cells. Resulting 3-D models for the most prominent structures, nuclear body and riboplasm, demonstrate their entirely membrane - enclosed nature. Immunogold localization of the FtsK protein also supports the internal organisation of G.obscuriglobus cells and their unique mechanism of cell division. We discuss how these new data expand our knowledge on bacterial cell biology and suggest evolutionary consequences of the findings.
    Full-text · Article · Mar 2014 · PLoS ONE
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    • "Given that most scientists pay more attention to the unique cell biological characteristics, few focus on the whole metabolic pathways of Planctomycetaceae family thus far. Such as, identification protein domains likely to be involved in morphogenesis, cell Division and signal transduction in Planctomycetes by comparative genomics [23]; the endocytosis process in G. obscuriglobus with eukaryotic membrane coat (MC)-like-protein-encoding genes [33]; the unusual peptidoglycan (PG)-free cell wall and ICM structure [18] and so on. Actually, the whole metabolic pathways analysis can help us explain the whole biological features well and provide more information to our research. "
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    ABSTRACT: The species in family Planctomycetaceae are ideal groups for investigating the origin of eukaryotes. Their cells are divided by a lipidic intracytoplasmic membrane and they share a number of eukaryote-like molecular characteristics. However, their genomic structures, potential abilities, and evolutionary status are still unknown. In this study, we searched for common protein families and a core genome/pan genome based on 11 sequenced species in family Planctomycetaceae. Then, we constructed phylogenetic tree based on their 832 common protein families. We also annotated the 11 genomes using the Clusters of Orthologous Groups database. Moreover, we predicted and reconstructed their core/pan metabolic pathways using the KEGG (Kyoto Encyclopedia of Genes and Genomes) orthology system. Subsequently, we identified genomic islands (GIs) and structural variations (SVs) among the five complete genomes and we specifically investigated the integration of two Planctomycetaceae plasmids in all 11 genomes. The results indicate that Planctomycetaceae species share diverse genomic variations and unique genomic characteristics, as well as have huge potential for human applications.
    Full-text · Article · Jan 2014 · PLoS ONE
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