The proteome of Mycoplasma pneumoniae, a supposedly “simple” cell

Abstract

This review covers progress in proteome research on Mycoplasma pneumoniae made over the last 5 years. This bacterium is one of the smallest known self-replicating bacteria. With fewer than 700 proposed proteins, it is well suited to a comprehensive proteome analysis. While all of the proposed genes are transcribed, thus far 620 proteins, about 90% of the predicted proteome, have been identified experimentally. To study the proteome organization of M. pneumoniae, 178 soluble protein complexes were isolated under non-denaturing conditions by tandem affinity chromatography and their composition determined by SDS-PAGE and mass spectrometry. The 62 homomultimeric and 116 heteromultimeric protein complexes could be classified according to 12 different COG functional categories. The complexes interacted with each other to some extent, forming larger assemblies. Protein complexes that were large enough and had specific structures (e.g. ribosomes or DNA-dependent RNA polymerase) were visible and countable in their natural environment by cryo-electron tomography. In addition to characterization of the soluble complexes, the analysis of the Triton X-100 insoluble fraction has a major role in the elucidation of the cytoskeleton-like structure, because by analogy with eukaryotic cells, almost all of the structural proteins involved in its formation, and enriched sub-cellular structures, can be found in this fraction.

Genome Reduction Promotes Increase in Protein Functional Complexity in Bacteria

“…Some of these novel interactions may be functionally beneficial, leading to rapid increases in the functional complexity of the proteins (Fernandez and Lynch 2011). For proteins in reduced genomes, this hypothesis predicts a general disposition to misfold, and to be multifunctional, as is true for Mycoplasmas (Wong and Houry 2004;Catrein and Herrmann 2011). In addition to drift, multitasking can also arise from biotic interactions among organisms, as is clear from the host-invasive and immune-system-evasive moonlighting activities of some core metabolic proteins in pathogens (Henderson and Martin 2011).…”

“…We hypothesize that in pathogens and other hostassociated bacteria with contracting genomes, the selective pressures on those remaining genes shift and induce the evolution of multitasking. Several proteins in bacterial pathogens have been shown to take on new activities, apparently to compensate for gene loss (Catrein and Herrmann 2011), and we suspect that as genome sizes decrease, there will be a broad trend to increase the functional repertoire of genes retained in these genomes. By examining the genome-wide protein-protein interaction (PPI) data for six bacterial genomes, we find that the surviving proteins in smaller genomes assume new functions, as reflected in the number and diversity of their interaction partners, thereby increasing their overall functional complexity during the process of genome reduction.…”

“…The loss of a gene might disable a pathway, thereby removing constraints on (and expediting the loss of) other genes in the inactivated pathway (Dagan et al 2006). Alternatively, the function of the lost genes might be complemented by others that can serve as compensatory alternatives (Pollack et al 2002;Catrein and Herrmann 2011;Wagner et al 2011). That the TCA cycle remains functional in M. tuberculosis despite the absence of KDH enzyme implies that another protein, which in this case is the multifunctional a-ketoglutarate decarboxylase (KGD), has taken on this compensatory role (Tian et al 2005;Wagner et al 2011).…”

Whole Surface Image of Mycoplasma mobile, Suggested by Protein Identification and Immunofluorescence Microscopy

“…Many studies focused on specific mycoplasmal surface proteins, including Gli521, Gli349, and MvspI of Mycoplasma mobile (1,28), P1 adhesin of Mycoplasma pneumoniae (25), and Mycoplasma arthritidis-derived mitogen (MAM) (20). On the other hand, many proteomic studies of mycoplasma species have been performed (5,6,10,11,18,21). However, "whole surface images," based on the integration of protein identification, quantification, and localization, have not been produced.…”

Bacterial Electron Transfer Chains Primed by Proteomics

“…Shotgun proteomics has been broadly used to make an inventory of the proteome of bacterial model species such as the Gram-negative Escherichia coli (Han & Lee, 2006;Krug et al, 2013), Gram-positive Bacillus subtilis (Becher, Büttner, Moche, Hessling, & Hecker, 2011;V€ olker & Hecker, 2005;Wolff et al, 2007), the industrially relevant Corynebacterium glutamicum (Fränzel et al, 2010;Fränzel & Wolters, 2011), pathogens such as Streptococcus pneumoniae , Mycobacterium tuberculosis (Calder, Soares, de Kock, & Blackburn, 2015;de Souza & Wiker, 2011;Mawuenyega et al, 2005) and Mycoplasma pneunomiae (Catrein & Herrmann, 2011), environmentally relevant Shewanella oneidensis (Brown, Romine, Schepmoes, Smith, & Lipton, 2010;Elias et al, 2005), the extreme thermophilic Archaeon Pyrococcus furiosus (Lee, Sevinsky, Bundy, Grunden, & Stephenson, 2009) and various others. As the result of extensive analyses of whole-cell lysates or subcellular fractions of these organisms, 50-60% of all proteins encoded in their genomes could be recovered.…”