Analysis of the Outer Membrane Proteome and Secretome of Bacteroides fragilis Reveals a Multiplicity of Secretion Mechanisms

Wilson, M.J.; Anderson, David E.; Bernstein, Harris

doi:10.1371/journal.pone.0117732

Cited by 67 publications

(65 citation statements)

References 81 publications

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“…Johnson, Sikora, Zielke, & Sandkvist, 2013;Renier et al, 2015;Zijnge, Kieselbach, & Oscarsson, 2012). These maps supported the evaluation of signal peptide algorithms (Leversen et al, 2009) and even suggested the presence of yet-unknown peptide transport systems (Wilson, Anderson, & Bernstein, 2015).…”

Section: Assembly Of Bacterial Respiratory Complexessupporting

confidence: 67%

Bacterial Electron Transfer Chains Primed by Proteomics

Wessels¹,

Almeida²,

Kartal³

et al. 2016

Advances in Bacterial Electron Transport Systems and Their Regulation

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Electron transport phosphorylation is the central mechanism for most prokaryotic species to harvest energy released in the respiration of their substrates as ATP. Microorganisms have evolved incredible variations on this principle, most of these we perhaps do not know, considering that only a fraction of the microbial richness is known. Besides these variations, microbial species may show substantial versatility in using respiratory systems. In connection herewith, regulatory mechanisms control the expression of these respiratory enzyme systems and their assembly at the translational and posttranslational levels, to optimally accommodate changes in the supply of their energy substrates. Here, we present an overview of methods and techniques from the field of proteomics to explore bacterial electron transfer chains and their regulation at levels ranging from the whole organism down to the Ångstrom scales of protein structures. From the survey of the literature on this subject, it is concluded that proteomics, indeed, has substantially contributed to our comprehending of bacterial respiratory mechanisms, often in elegant combinations with genetic and biochemical approaches. However, we also note that advanced proteomics offers a wealth of opportunities, which have not been exploited at all, or at best underexploited in hypothesis-driving and hypothesis-driven research on bacterial bioenergetics. Examples obtained from the related area of mitochondrial oxidative phosphorylation research, where the application of advanced proteomics is more common, may illustrate these opportunities.

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Section: Assembly Of Bacterial Respiratory Complexessupporting

confidence: 67%

Bacterial Electron Transfer Chains Primed by Proteomics

Wessels¹,

Almeida²,

Kartal³

et al. 2016

Advances in Bacterial Electron Transport Systems and Their Regulation

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“…To determine whether the LES identified in C. canimorsus would be conserved in other Bacteroidetes , we took advantage of the recently published B. fragilis NCTC 9343 surfome study (44) and performed an in silico analysis on the N termini of the identified surface lipoproteins (see Fig. S5A in the supplemental material).…”

Section: Resultsmentioning

confidence: 99%

Identification of a New Lipoprotein Export Signal in Gram-Negative Bacteria

Lauber

Cornelis

Renzi

2016

mBio

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Bacteria of the phylum Bacteroidetes, including commensal organisms and opportunistic pathogens, harbor abundant surface-exposed multiprotein membrane complexes (Sus-like systems) involved in carbohydrate acquisition. These complexes have been mostly linked to commensalism, and in some instances, they have also been shown to play a role in pathogenesis. Sus-like systems are mainly composed of lipoproteins anchored to the outer membrane and facing the external milieu. This lipoprotein localization is uncommon in most studied Gram-negative bacteria, while it is widespread in Bacteroidetes. Little is known about how these complexes assemble and particularly about how lipoproteins reach the bacterial surface. Here, by bioinformatic analyses, we identify a lipoprotein export signal (LES) at the N termini of surface-exposed lipoproteins of the human pathogen Capnocytophaga canimorsus corresponding to K-(D/E)2 or Q-A-(D/E)2. We show that, when introduced in sialidase SiaC, an intracellular lipoprotein, this signal is sufficient to target the protein to the cell surface. Mutational analysis of the LES in this reporter system showed that the amino acid composition, position of the signal sequence, and global charge are critical for lipoprotein surface transport. These findings were further confirmed by the analysis of the LES of mucinase MucG, a naturally surface-exposed C. canimorsus lipoprotein. Furthermore, we identify a LES in Bacteroides fragilis and Flavobacterium johnsoniae surface lipoproteins that allow C. canimorsus surface protein exposure, thus suggesting that Bacteroidetes share a new bacterial lipoprotein export pathway that flips lipoproteins across the outer membrane.

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“…3A; Dataset S1, Table S4). Three of these proteins are homologs of the secreted proteobacterial T6SS structural proteins Hcp [also observed in a recent study (16)] and VgrG, and the fourth contains a PAARrepeat domain typical of T6SS adaptors (9,10). Of the two remaining proteins, BF9343_1937 lacks any known T6S effector domains, and BF9343_1928 contains a MIX domain found in other T6SS effectors (17).…”

Section: B Fragilis Strains Encode Extensive Variation In Effector/imentioning

confidence: 69%

Human symbionts inject and neutralize antibacterial toxins to persist in the gut

Wexler

Bao

Whitney

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

180

203

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The human gut microbiome is a dynamic and densely populated microbial community that can provide important benefits to its host. Cooperation and competition for nutrients among its constituents only partially explain community composition and interpersonal variation. Notably, certain human-associated Bacteroidetes—one of two major phyla in the gut—also encode machinery for contact-dependent interbacterial antagonism, but its impact within gut microbial communities remains unknown. Here we report that prominent human gut symbionts persist in the gut through continuous attack on their immediate neighbors. Our analysis of just one of the hundreds of species in these communities reveals 12 candidate antibacterial effector loci that can exist in 32 combinations. Through the use of secretome studies, in vitro bacterial interaction assays and multiple mouse models, we uncover strain-specific effector/immunity repertoires that can predict interbacterial interactions in vitro and in vivo, and find that some of these strains avoid contact-dependent killing by accumulating immunity genes to effectors that they do not encode. Effector transmission rates in live animals can exceed 1 billion events per minute per gram of colonic contents, and multiphylum communities of human gut commensals can partially protect sensitive strains from these attacks. Together, these results suggest that gut microbes can determine their interactions through direct contact. An understanding of the strategies human gut symbionts have evolved to target other members of this community may provide new approaches for microbiome manipulation.

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Analysis of the Outer Membrane Proteome and Secretome of Bacteroides fragilis Reveals a Multiplicity of Secretion Mechanisms

Cited by 67 publications

References 81 publications

Bacterial Electron Transfer Chains Primed by Proteomics

Bacterial Electron Transfer Chains Primed by Proteomics

Identification of a New Lipoprotein Export Signal in Gram-Negative Bacteria

Human symbionts inject and neutralize antibacterial toxins to persist in the gut

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