Twitch or swim: towards the understanding of prokaryotic motion based on the type IV pilus blueprint

Daum, Bertram; Gold, Vicki A. M.

doi:10.1515/hsz-2018-0157

Cited by 20 publications

(19 citation statements)

References 78 publications

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“…Tfp are flexible, surface-exposed, hairlike structures found in both bacteria and archaea (9). Much of the knowledge on the biology of Tfp was generated from studies on Gram-negative pathogens (10), in which Tfp are often critical for their pathogenic capacity.…”

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confidence: 99%

Molecular and Functional Analysis of the Type IV Pilus Gene Cluster in Streptococcus sanguinis SK36

Chen

Chiang

Tseng

et al. 2019

Appl Environ Microbiol

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Streptococcus sanguinis, dominant in the oral microbiome, is the only known streptococcal species possessing a pil gene cluster for the biosynthesis of type IV pili (Tfp). Although this cluster is commonly present in the genome of S. sanguinis, most of the strains do not express Tfp-mediated twitching motility. Thus, this study was designed to investigate the biological functions encoded by the cluster in the twitching-negative strain S. sanguinis SK36. We found that the cluster was transcribed as an operon, with three promoters located 5= to the cluster and one in the intergenic region between SSA_2307 and SSA_2305. Studies using promoter-cat fusion strains revealed that the transcription of the cluster was mainly driven by the distal 5= promoter, which is located more than 800 bases 5= to the first gene of the cluster, SSA_2318. Optimal expression of the cluster occurred at the early stationary growth phase in a CcpA-dependent manner, although a CcpA-binding consensus is absent in the promoter region. Expression of the cluster resulted in a short hairlike surface structure under transmission electron microscopy. Deletion of the putative pilin genes (SSA_2313 to SSA_2315) abolished the biosynthesis of this structure and significantly reduced the adherence of SK36 to HeLa and SCC-4 cells. Mutations in the pil genes downregulated biofilm formation by S. sanguinis SK36. Taken together, the results demonstrate that Tfp of SK36 are important for host cell adherence, but not for motility, and that expression of the pil cluster is subject to complex regulation. IMPORTANCE The proteins and assembly machinery of the type IV pili (Tfp) are conserved throughout bacteria and archaea, and yet the function of this surface structure differs from species to species and even from strain to strain. As seen in Streptococcus sanguinis SK36, the expression of the Tfp gene cluster results in a hairlike surface structure that is much shorter than the typical Tfp. This pilus is essential for the adherence of SK36 but is not involved in motility. Being a member of the highly diverse dental biofilm, perhaps S. sanguinis could more effectively utilize this structure to adhere to host cells and to interact with other microbes within the same niche.

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Molecular and Functional Analysis of the Type IV Pilus Gene Cluster in Streptococcus sanguinis SK36

Chen

Chiang

Tseng

et al. 2019

Appl Environ Microbiol

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“…Experiment 4F1% resulted in the up to 3.8-fold upregulation of the expression of 11 type IV pilus genes (GSU2029-GSU2039). Type IV pili have multiple functions in bacteria, including cell communication, adhesion, biofilm formation and cell motility (16,17). Motility is caused by cells protruding pilus fibres whose tips attach on a surface and subsequently retracting the pilus again, pulling the cell body forward (18).…”

Section: Discussionmentioning

confidence: 99%

“…While the above mentioned type IV pili genes have been investigated by several additional studies (21–23), the genes encoded by GSU2029 to GSU2039 have to our knowledge not been investigated more closely in Geobacter species. GSU2029 to GSU2039 include genes for PilM, PilN, PilO and PilP, which are thought to be part of the assembly responsible for pilus protrusion and retraction in G. sulfurreducens (19) as they serve this function in other bacteria (16,18). Some of the remaining genes encode for PilX-2, PilW-2, PilV-2 and FimU, which represent minor pilins.…”

Section: Discussionmentioning

confidence: 99%

Quantification of microaerobic growth ofGeobacter sulfurreducens

Engel

VorlaÌˆnder

Biedendieck

et al. 2019

Preprint

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20 Geobacter sulfurreducens was originally considered a strict anaerobe. However, this 21 bacterium was later shown to not only tolerate exposure to oxygen but also to use it as 22 terminal electron acceptor. Research performed has so far only revealed the general ability of 23 G. sulfurreducens to reduce oxygen, but the oxygen uptake rate has not been quantified yet, 24 nor has evidence been provided as to how the bacterium achieves oxygen reduction.25 Therefore, microaerobic growth of G. sulfurreducens was investigated here with better 26 defined operating conditions as previously performed and a transcriptome analysis was 27 performed to elucidate possible metabolic mechanisms important for oxygen reduction in G.28 sulfurreducens. The investigations revealed that cell growth with oxygen is possible to the 29 same extent as with fumarate if the maximum specific oxygen uptake rate (sOUR) of 30 95 mg O2 g CDW -1 h -1 is not surpassed. Hereby, the entire amount of introduced oxygen is 31 reduced. When oxygen concentrations are too high, cell growth is completely inhibited and 32 there is no partial oxygen consumption. Transcriptome analysis suggests a menaquinol 33 oxidase to be the enzyme responsible for oxygen reduction. Transcriptome analysis has 34 further revealed three different survival strategies, depending on the oxygen concentration 35 present. When prompted with small amounts of oxygen, G. sulfurreducens will try to escape 36 the microaerobic area; if oxygen concentrations are higher, cells will focus on rapid and 37 complete oxygen reduction coupled to cell growth; and ultimately cells will form protective 38 layers if a complete reduction becomes impossible. The results presented here have important 39 implications for understanding how G. sulfurreducens survives exposure to oxygen. 40 41 42 43 Introduction 44 Geobacter sulfurreducens, a δ-proteobacterium found in subsurface environments, was 45 originally reported to be a strict anaerobe (1). However, it was later shown that this bacterium 46 can grow with oxygen as terminal electron acceptor when 5 % of oxygen or less are added to 47 the headspace of cultivation flasks (2). But this study did not investigate dissolved oxygen 48 concentrations reached in the liquid phase under these conditions (2). Further, the analysis of 49 the genome of G. sulfurreducens revealed several enzymes that could be involved in the 50 reduction of oxygen (3). The expression of many of the corresponding genes is regulated by 51 the RpoS regulon in G. sulfurreducens, which was shown to be inevitable for cell growth with 52 oxygen (4). Part of the RpoS regulon are genes for the cytochrome c oxidase, which is 53 thought to be most likely responsible for cell growth with oxygen, but genes for a cytochrome 54 d ubiquinol oxidase and a rubredoxin-oxygen oxidoreductase have also been found to be 55 regulated by RpoS and encode for enzymes that may play a role in oxygen reduction (3,5).56 The gene for a cytochrome d ubiquinol oxidase has also been found upregulated in Geobacter 5...

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“…Various surface-exposed molecules, such as adhesins, S-layer proteins, LPS, or capsular polysaccharides, offer a means for bacterial symbionts and pathogens to interact with their eukaryotic hosts in antigen presentation and receptor-mediated adhesion (8). Pili and flagella participate in adhesion, mechanotransduction, transfer of genetic material during conjugation, and bacterial motility (9)(10)(11)(12)(13). Finally, integral membrane proteins traversing the PM or OM take part in many crucial functions, such as nutrient uptake, antibiotic extrusion, ATP synthesis, stress transduction, conjugation, and protein secretion (14).…”

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confidence: 99%

Scratching the Surface: Bacterial Cell Envelopes at the Nanoscale

Viljoen

Foster

Fantner

et al. 2020

mBio

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The bacterial cell envelope is essential for viability, the environmental gatekeeper and first line of defense against external stresses. For most bacteria, the envelope biosynthesis is also the site of action of some of the most important groups of antibiotics. It is a complex, often multicomponent structure, able to withstand the internally generated turgor pressure. Thus, elucidating the architecture and dynamics of the cell envelope is important, to unravel not only the complexities of cell morphology and maintenance of integrity but also how interventions such as antibiotics lead to death. To address these questions requires the capacity to visualize the cell envelope in situ via high-spatial resolution approaches. In recent years, atomic force microscopy (AFM) has brought novel molecular insights into the assembly, dynamics, and functions of bacterial cell envelopes. The ultrafine resolution and physical sensitivity of the technique have revealed a wealth of ultrastructural features that are invisible to traditional optical microscopy techniques or imperceptible in their true physiological state by electron microscopy. Here, we discuss recent progress in our use of AFM imaging for understanding the architecture and dynamics of the bacterial envelope. We survey recent studies that demonstrate the power of the technique to observe isolated membranes and live cells at (sub)nanometer resolution and under physiological conditions and to track in vitro structural dynamics in response to growth or to drugs.

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Twitch or swim: towards the understanding of prokaryotic motion based on the type IV pilus blueprint

Cited by 20 publications

References 78 publications

Molecular and Functional Analysis of the Type IV Pilus Gene Cluster in Streptococcus sanguinis SK36

Molecular and Functional Analysis of the Type IV Pilus Gene Cluster in Streptococcus sanguinis SK36

Quantification of microaerobic growth ofGeobacter sulfurreducens

Scratching the Surface: Bacterial Cell Envelopes at the Nanoscale

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