Conserved Terminal Organelle Morphology and Function in Mycoplasma penetrans and Mycoplasma iowae

Jurkovic, Dominika A.; Newman, Jaime T.; Balish, Mitchell F.

doi:10.1128/jb.00060-12

Cited by 15 publications

(28 citation statements)

References 36 publications

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“…2), as revealed by overlaying phase-contrast images and images of the DNA stained with 4=,6-diamidino-2-phenylindole (DAPI) (Fig. 2G) (7). The mean length of the nucleoid-free zones was 380 Ϯ 140 nm.…”

Section: Resultsmentioning

confidence: 99%

“…Treatment of M. penetrans cells attached to plastic with the nonionic detergent Triton X-100 results in solubilization of a large amount of cellular material, leaving behind discrete detergent-insoluble objects with a range of dimensions, as visualized by scanning electron microscopy (SEM) (Fig. 1C) (7). Unlike the AO structures obtained similarly from species of the M. pneumoniae cluster (23), treatment with DNase had no effect on the appearance of these objects (data not shown), indicating that they did not contain significant amounts of DNA.…”

Section: Resultsmentioning

confidence: 99%

“…The major focus of studies of M. penetrans has been its putative role as an AIDS cofactor (9)(10)(11)(12). We showed previously that the M. penetrans AO contains material distinct in structure from that of M. pneumoniae and M. mobile (7). Furthermore, M. penetrans lacks any homologs of the AO structural proteins of M. pneumoniae or M. mobile (4,13,14).…”

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confidence: 99%

“…Mycoplasma penetrans is another species that has a polar AO, representing a third mycoplasma phylogenetic cluster (5)(6)(7). M. penetrans is best known for its association with AIDS patients, in whom it is commonly found in the urogenital tract, but it has also been isolated from an HIV-negative patient with antiphospholipid syndrome (5,6,8).…”

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The Variable Internal Structure of the Mycoplasma penetrans Attachment Organelle Revealed by Biochemical and Microscopic Analyses: Implications for Attachment Organelle Mechanism and Evolution

et al. 2017

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Although mycoplasmas have small genomes, many of them, including the HIV-associated opportunist Mycoplasma penetrans, construct a polar attachment organelle (AO) that is used for both adherence to host cells and gliding motility. However, the irregular phylogenetic distribution of similar structures within the mycoplasmas, as well as compositional and ultrastructural differences among these AOs, suggests that AOs have arisen several times through convergent evolution. We investigated the ultrastructure and protein composition of the cytoskeleton-like material of the M. penetrans AO with several forms of microscopy and biochemical analysis, to determine whether the M. penetrans AO was constructed at the molecular level on principles similar to those of other mycoplasmas, such as Mycoplasma pneumoniae and Mycoplasma mobile. We found that the M. penetrans AO interior was generally dissimilar from that of other mycoplasmas, in that it exhibited considerable heterogeneity in size and shape, suggesting a gel-like nature. In contrast, several of the 12 potential protein components identified by mass spectrometry of M. penetrans detergent-insoluble proteins shared certain distinctive biochemical characteristics with M. pneumoniae AO proteins, although not with M. mobile proteins. We conclude that convergence between M. penetrans and M. pneumoniae AOs extends to the molecular level, leading to the possibility that the less organized material in both M. pneumoniae and M. penetrans is the substance principally responsible for the organization and function of the AO.IMPORTANCE Mycoplasma penetrans is a bacterium that infects HIV-positive patients and may contribute to the progression of AIDS. It attaches to host cells through a structure called an AO, but it is not clear how it builds this structure. Our research is significant not only because it identifies the novel protein components that make up the material within the AO that give it its structure but also because we find that the M. penetrans AO is organized unlike AOs from other mycoplasmas, suggesting that similar structures have evolved multiple times. From this work, we derive some basic principles by which mycoplasmas, and potentially all organisms, build structures at the subcellular level.KEYWORDS Mycoplasma, cytoskeleton, electron microscopy, evolution, fractionation, mass spectrometry, transcriptomics

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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The Variable Internal Structure of the Mycoplasma penetrans Attachment Organelle Revealed by Biochemical and Microscopic Analyses: Implications for Attachment Organelle Mechanism and Evolution

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“…It is conceivable that M. mobile and M. pneumoniae have simply diverged very greatly, rendering homology between these elements unrecognizable. On the other hand, gliding motility of Mycoplasma penetrans, which itself lacks homologs of AO proteins of both M. mobile and M. pneumoniae and has an AO of different appearance from those of both species (75), is relatively insensitive to lethal amounts of arsenate (76), which rapidly depletes cellular ATP, leaving M. mobile nearly motionless within seconds (77). Instead, the movement of M. penetrans merely slows gradually over time, suggesting that maintenance of the motor is the only ATP-dependent feature of motility.…”

Section: Yet Another Gliding Motility Mechanismmentioning

confidence: 99%

Mycoplasma pneumoniae, an Underutilized Model for Bacterial Cell Biology

Balish

2014

J Bacteriol

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In recent decades, bacterial cell biology has seen great advances, and numerous model systems have been developed to study a wide variety of cellular processes, including cell division, motility, assembly of macromolecular structures, and biogenesis of cell polarity. Considerable attention has been given to these model organisms, which include Escherichia coli, Bacillus subtilis, Caulobacter crescentus, and Myxococcus xanthus. Studies of these processes in the pathogenic bacterium Mycoplasma pneumoniae and its close relatives have also been carried out on a smaller scale, but this work is often overlooked, in part due to this organism's reputation as minimalistic and simple. In this minireview, I discuss recent work on the role of the M. pneumoniae attachment organelle (AO), a structure required for adherence to host cells, in these processes. The AO is constructed from proteins that generally lack homology to those found in other organisms, and this construction occurs in coordination with cell cycle events. The proteins of the M. pneumoniae AO share compositional features with proteins with related roles in model organisms. Once constructed, the AO becomes activated for its role in a form of gliding motility whose underlying mechanism appears to be distinct from that of other gliding bacteria, including Mycoplasma mobile. Together with the FtsZ cytoskeletal protein, motility participates in the cell division process. My intention is to bring this deceptively complex organism into alignment with the better-known model systems. Mycoplasmas have a long-standing reputation for being something they are not: exceptionally simple. The common term "mycoplasma" encompasses the bacteria of the genera within the phylum Tenericutes and the class Mollicutes (1). These organisms are most distinctively characterized by the absence of any cell wall material, with the cell envelope consisting of a single lipid bilayer and its associated proteins and carbohydrates. Having undergone reductive evolution from Firmicutes ancestors (2), mycoplasma genomes are less complex than those of other bacteria that are capable of being grown axenically in a laboratory setting, which has led to their service as model organisms for studying genomes in a minimal setting (3) and as platforms for synthetic biology (4).This reduced genomic complexity has led to a perception that mycoplasmas are aberrantly uncomplicated organisms whose value to researchers, beyond dealing with the diseases that they cause, is only as simplified models for cell structure and genome analysis. But since the small genome size results from loss of major anabolic pathways and reduction in the complexity of gene expression regulation, mycoplasmas can still serve as models for other kinds of complex cellular processes. These include genesis of cell polarity, assembly of macromolecular structures, cell division, adherence, and motility.The human pathogen Mycoplasma pneumoniae (5) is particularly instructive. M. pneumoniae cells feature an attachment organelle (AO) or termina...

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Mycoplasma

Brown

May

Bradbury

et al. 2018

Bergey's Manual of Systematics of Archaea and Bacteria

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My.co.plas'ma. Gr. masc. n. myces a fungus; Gr. neut. n. plasma something formed or molded, a form; N.L. neut. n. Mycoplasma fungus form. Tenericutes / Mollicutes / Mycoplasmatales / Mycoplasmataceae / Mycoplasma Bacteria in the genus Mycoplasma are small (300–800 nm in diameter) pleomorphic cells devoid of a cell wall. Culturable species usually form very small (<1 mm) umbonate colonies on agar. Their use of the codon UGA to encode tryptophan is a distinctive characteristic of all species examined to date. As a consequence of their small (usually 0.5–1.5 Mb) genomes they have limited intermediary metabolism and are nutritionally fastidious, requiring exogenous sugars or arginine, cholesterol or other sterols, peptides, and free nucleic acids for axenic growth. In nature, all species are obligate commensals or parasites with varying degrees of specificity for a wide range of vertebrate hosts. The type species Mycoplasma mycoides subsp. mycoides and Mycoplasma capricolum subsp. capripneumoniae are highly virulent animal pathogens subject to strict international regulations, but the genus is perhaps better known for Mycoplasma pneumoniae , the agent of primary atypical “walking” pneumonia in humans. The relative biological simplicity of mycoplasmas confers significant advantages for current proteomics, metabolomics, synthetic genomics, and systems biology research. For example, the recent chemical synthesis and transplantation of intact chromosomes demonstrated that it is possible to enliven a mycoplasma fully capable of autonomous replication with an artificially constructed genome. DNA G + C content ( mol %): 23–40. Type species : Mycoplasma mycoides (Borrel, Dujardin‐Beaumetz, Jeantet and Jouan 1910) Freundt 1955, 73 ( Asterococcus mycoides Borrel, Dujardin‐Beaumetz, Jeantet and Jouan 1910, 179).

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Conserved Terminal Organelle Morphology and Function in Mycoplasma penetrans and Mycoplasma iowae

Cited by 15 publications

References 36 publications

The Variable Internal Structure of the Mycoplasma penetrans Attachment Organelle Revealed by Biochemical and Microscopic Analyses: Implications for Attachment Organelle Mechanism and Evolution

The Variable Internal Structure of the Mycoplasma penetrans Attachment Organelle Revealed by Biochemical and Microscopic Analyses: Implications for Attachment Organelle Mechanism and Evolution

Mycoplasma pneumoniae, an Underutilized Model for Bacterial Cell Biology

Mycoplasma

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