scholarly journals Heterogeneity in surface sensing produces a division of labor in Pseudomonas aeruginosa populations

2019 ◽  
Author(s):  
Catherine R. Armbruster ◽  
Calvin K. Lee ◽  
Jessica Parker-Gilham ◽  
Jaime de Anda ◽  
Aiguo Xia ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Division Of Labor ◽  
Bacterial Species ◽  
Biofilm Growth ◽  
Surface Attachment ◽  
Sensing Systems ◽  
Current Thinking ◽  
Surface Exploration ◽  
Surface Sensing ◽  
Second Messenger Signaling

AbstractThe second messenger signaling molecule cyclic diguanylate monophosphate (c-di-GMP) drives the transition from planktonic to biofilm growth in many bacterial species. Pseudomonas aeruginosa has two surface sensing systems that produce c-di-GMP in response to surface adherence. The current thinking in the field is that once cells attach to a surface, they uniformly respond with elevated c-di-GMP. Here, we describe how the Wsp system generates heterogeneity in surface sensing, resulting in two physiologically distinct subpopulations of cells. One subpopulation has elevated c-di-GMP and produces biofilm matrix, serving as the founders of initial microcolonies. The other subpopulation has low c-di-GMP and engages in surface motility, allowing for exploration of the surface. We also show that this heterogeneity strongly correlates to surface behavior for descendent cells. Together, our results suggest that after surface attachment, P. aeruginosa engages in a division of labor that persists across generations, accelerating early biofilm formation and surface exploration.

scholarly journals Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Catherine R Armbruster ◽  
Calvin K Lee ◽  
Jessica Parker-Gilham ◽  
Jaime de Anda ◽  
Aiguo Xia ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Division Of Labor ◽  
Bacterial Species ◽  
Biofilm Growth ◽  
Surface Attachment ◽  
Sensing Systems ◽  
Current Thinking ◽  
Surface Exploration ◽  
Surface Sensing ◽  
Second Messenger Signaling

The second messenger signaling molecule cyclic diguanylate monophosphate (c-di-GMP) drives the transition between planktonic and biofilm growth in many bacterial species. Pseudomonas aeruginosa has two surface sensing systems that produce c-di-GMP in response to surface adherence. Current thinking in the field is that once cells attach to a surface, they uniformly respond by producing c-di-GMP. Here, we describe how the Wsp system generates heterogeneity in surface sensing, resulting in two physiologically distinct subpopulations of cells. One subpopulation has elevated c-di-GMP and produces biofilm matrix, serving as the founders of initial microcolonies. The other subpopulation has low c-di-GMP and engages in surface motility, allowing for exploration of the surface. We also show that this heterogeneity strongly correlates to surface behavior for descendent cells. Together, our results suggest that after surface attachment, P. aeruginosa engages in a division of labor that persists across generations, accelerating early biofilm formation and surface exploration.

scholarly journals Author response: Heterogeneity in surface sensing suggests a division of labor in Pseudomonas aeruginosa populations

2019 ◽  
Author(s):  
Catherine R Armbruster ◽  
Calvin K Lee ◽  
Jessica Parker-Gilham ◽  
Jaime de Anda ◽  
Aiguo Xia ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Division Of Labor ◽  
Author Response ◽  
Surface Sensing

scholarly journals Social Cooperativity of Bacteria during Reversible Surface Attachment in Young Biofilms: a Quantitative Comparison of Pseudomonas aeruginosa PA14 and PAO1

mBio ◽  
2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Calvin K. Lee ◽  
Jérémy Vachier ◽  
Jaime de Anda ◽  
Kun Zhao ◽  
Amy E. Baker ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Stochastic Model ◽  
Bacterial Biofilm ◽  
Population Increase ◽  
Pivotal Phase ◽  
Surface Attachment ◽  
Content Type ◽  
Cellular Behavior ◽  
Bacterial Surface ◽  
Surface Sensing

ABSTRACT What are bacteria doing during “reversible attachment,” the period of transient surface attachment when they initially engage a surface, besides attaching themselves to the surface? Can an attaching cell help any other cell attach? If so, does it help all cells or employ a more selective strategy to help either nearby cells (spatial neighbors) or its progeny (temporal neighbors)? Using community tracking methods at the single-cell resolution, we suggest answers to these questions based on how reversible attachment progresses during surface sensing for Pseudomonas aeruginosa strains PAO1 and PA14. Although PAO1 and PA14 exhibit similar trends of surface cell population increase, they show unanticipated differences when cells are considered at the lineage level and interpreted using the quantitative framework of an exactly solvable stochastic model. Reversible attachment comprises two regimes of behavior, processive and nonprocessive, corresponding to whether cells of the lineage stay on the surface long enough to divide, or not, before detaching. Stark differences between PAO1 and PA14 in the processive regime of reversible attachment suggest the existence of two surface colonization strategies. PAO1 lineages commit quickly to a surface compared to PA14 lineages, with early c-di-GMP-mediated exopolysaccharide (EPS) production that can facilitate the attachment of neighbors. PA14 lineages modulate their motility via cyclic AMP (cAMP) and retain memory of the surface so that their progeny are primed for improved subsequent surface attachment. Based on the findings of previous studies, we propose that the differences between PAO1 and PA14 are potentially rooted in downstream differences between Wsp-based and Pil-Chp-based surface-sensing systems, respectively. IMPORTANCE The initial pivotal phase of bacterial biofilm formation known as reversible attachment, where cells undergo a period of transient surface attachment, is at once universal and poorly understood. What is more, although we know that reversible attachment culminates ultimately in irreversible attachment, it is not clear how reversible attachment progresses phenotypically, as bacterial surface-sensing circuits fundamentally alter cellular behavior. We analyze diverse observed bacterial behavior one family at a time (defined as a full lineage of cells related to one another by division) using a unifying stochastic model and show that our findings lead to insights on the time evolution of reversible attachment and the social cooperative dimension of surface attachment in PAO1 and PA14 strains.

scholarly journals Truncation in the core oligosaccharide of lipopolysaccharide affects flagella-mediated motility in Pseudomonas aeruginosa PAO1 via modulation of cell surface attachment

Microbiology ◽  
2009 ◽  
Vol 155 (10) ◽  
pp. 3449-3460 ◽  
Author(s):  
Theresa Lindhout ◽  
Peter C. Y. Lau ◽  
Dyanne Brewer ◽  
Joseph S. Lam
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Cell Surface ◽  
Bacterial Species ◽  
Soft Agar ◽  
Wild Type ◽  
Core Oligosaccharide ◽  
Swarming Motility ◽  
Surface Attachment ◽  
Abiotic Surfaces ◽  
Isogenic Mutants

In many Gram-negative bacterial species, rough strains producing truncated lipopolysaccharide (LPS) generally exhibit defects in motility compared with smooth strains. However, the role that LPS plays in bacterial motility is not well understood. The goal of this study was to examine the relationship between LPS defects and motility of Pseudomonas aeruginosa. P. aeruginosa wild-type strain PAO1 and three isogenic mutants with defects in the rmlC, migA and wapR genes and producing truncated core oligosaccharide were investigated in terms of motility, attachment to glass and flagella expression. Compared with the wild-type, the three mutants showed significant retardation in both swarming motility on 0.5 % soft-agar plates and swimming motility on 0.3 % soft-agar plates. Moreover, attachment to abiotic surfaces was observed to be stronger in these mutants. The assembly of flagella appeared to be intact in these strains and the ability of individual cells to swim was unaffected. Flagellin proteins prepared from mutants rmlC and rmd, defective in the production of TDP-l-rhamnose and GDP-d-rhamnose, respectively, were compared and a change in molecular mass was observed only in the rmlC mutant. These data indicated that l-rhamnose, and not its enantiomer, d-rhamnose, is incorporated into the flagellin glycan of P. aeruginosa PAO1. The nucleotide-activated sugar precursor TDP-l-rhamnose is therefore shared between LPS biosynthesis and flagellin glycosylation in P. aeruginosa PAO1. Our results suggest that although biochemical precursors are shared by LPS and flagellin glycan biosynthesis, LPS truncations probably alter flagella-mediated motility in P. aeruginosa by modulating cell-surface attachment but not flagella synthesis.

scholarly journals Surfing Motility: a Conserved yet Diverse Adaptation among Motile Bacteria

2018 ◽  
Vol 200 (23) ◽  
Author(s):  
Evelyn Sun ◽  
Sijie Liu ◽  
Robert E. W. Hancock
Keyword(s):  
Escherichia Coli ◽  
Pseudomonas Aeruginosa ◽  
Quorum Sensing ◽  
Broad Spectrum ◽  
Proteus Mirabilis ◽  
Salmonella Enterica ◽  
Bacterial Species ◽  
Content Type ◽  
Adaptive Resistance ◽  
Sensing Systems

ABSTRACTBacterial rapid surfing motility is a novel surface adaptation ofPseudomonas aeruginosain the presence of the glycoprotein mucin. Here, we show that other Gram-negative motile bacterial species, includingEscherichia coli,Salmonella enterica,Vibrio harveyi,Enterobacter cloacae, andProteus mirabilis, also exhibit the physical characteristics of surfing on the surface of agar plates containing 0.4% mucin, where surfing motility was generally more rapid and less dependent on medium viscosity than was swimming motility. As previously observed inPseudomonas aeruginosa, all surfing species exhibited some level of broad-spectrum adaptive resistance, although the antibiotics to which they demonstrated surfing-mediated resistance differed. Surfing motility inP. aeruginosawas found to be dependent on the quorum-sensing systems of this organism; however, this aspect was not conserved in other tested bacterial species, includingV. harveyiandS. enterica, as demonstrated by assaying specific quorum-sensing mutants. Thus, rapid surfing motility is a complex surface growth adaptation that is conserved in several motile bacteria, involves flagella, and leads to diverse broad-spectrum antibiotic resistance, but it is distinct in terms of dependence on quorum sensing.IMPORTANCEThis study showed for the first time that surfing motility, a novel form of surface motility first discovered inPseudomonas aeruginosaunder artificial cystic fibrosis conditions, including the presence of high mucin content, is conserved in other motile bacterial species known to be mucosa-associated, includingEscherichia coli,Salmonella enterica, andProteus mirabilis. Here, we demonstrated that key characteristics of surfing, including the ability to adapt to various viscous environments and multidrug adaptive resistance, are also conserved. Using mutagenesis assays, we also identified the importance of all three known quorum-sensing systems, Las, Rhl, and Pqs, inP. aeruginosain regulating surfing motility, and we also observed a conserved dependence of surfing on flagella in certain species.

scholarly journals Fine tuning cyclic-di-GMP signaling in Pseudomonas aeruginosa using the type 4 pili alignment complex

2020 ◽  
Author(s):  
Shanice S. Webster ◽  
Calvin K. Lee ◽  
William C. Schmidt ◽  
Gerard C. L. Wong ◽  
George A. O’Toole
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Biofilm Formation ◽  
Cell Tracking ◽  
Dynamic Range ◽  
Fine Tuning ◽  
Bimolecular Fluorescence Complementation ◽  
Initial Surface ◽  
Biofilm Growth ◽  
Surface Sensing ◽  
Fine Tune

AbstractTo initiate biofilm formation it is critical for bacteria to sense a surface and respond precisely. Type 4 pili (T4P) have been shown to be important in surface sensing, however, mechanism(s) driving downstream changes important for the switch to biofilm growth have not been clearly defined. Here, using macroscopic bulk assays and single cell tracking analyses of Pseudomonas aeruginosa, we uncover a new role of the T4P alignment complex protein, PilO, in modulating the activity of the diguanylate cyclase (DGC) SadC. Two hybrid and bimolecular fluorescence complementation assays show that PilO physically interacts with SadC and that the PilO-SadC interaction inhibits SadC’s activity resulting in decreased biofilm formation and increased motility. We show that disrupting the PilO-SadC interaction contributes to greater variation of cyclic-di-GMP levels among cells, thereby increasing cell-to-cell heterogeneity in the levels of this signal. Thus, this work shows that P. aeruginosa uses a component of the T4P scaffold to fine-tune the levels of this nucleotide signal during surface commitment. Finally, given our previous findings linking SadC to the flagellar machinery, we propose that this DGC acts as a bridge to integrate T4P and flagellar-derived input signals during initial surface engagement.Significance StatementT4P of P. aeruginosa are important for surface sensing and regulating intracellular cyclic-di-GMP levels. This work identifies a new role for the T4P alignment complex, previously known for its role in supporting pili biogenesis, in surface-dependent signaling. Furthermore, our findings indicate that P. aeruginosa uses a single DGC, via a complex web of protein-protein interactions, to integrate signaling through the T4P and the flagellar motor to fine-tune cyclic-di-GMP levels. A key implication of this work is that more than just regulating signal levels, cells must modulate the dynamic range of cyclic-di-GMP to precisely control the transition to a biofilm lifestyle.

scholarly journals An expanding bacterial colony forms a depletion zone with growing droplets

2020 ◽  
Author(s):  
H. Ma ◽  
J. Bell ◽  
J.X. Tang
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Bacterial Growth ◽  
Fluid Dynamic ◽  
Bacterial Species ◽  
Cell Interaction ◽  
Water Evaporation ◽  
Depletion Zone ◽  
Biofilm Growth ◽  
Bacterial Colony ◽  
Pattern Dynamics

AbstractMany species of bacteria have developed means to spread on solid surfaces. This study focuses on the expansion of Pseudomonas aeruginosa on an agar gel surface. We report the occurrence and spread of a depletion zone, where the layer of bacteria on the agar becoming thinner. The depletion zone occurs within an expanded colony under conditions of minimal water evaporation. It is colocalized with a higher concentration of rhamnolipids, the biosurfactants that are produced by the bacteria and accumulate in the older region of the colony. With continued growth in bacterial population, dense droplets occur and coalesce in the depletion zone, displaying remarkable fluid dynamic behavior. Whereas expansion of a central depletion zone requires activities of live bacteria, new zones can be seeded by adding rhamnolipids. These depletion zones due to the added surfactants expand quickly, even on plates covered by bacteria that have been killed by ultraviolet light. We propose a model to account for the observed properties, taking into consideration bacterial growth and secretion, osmotic swelling, fluid volume expansion, cell-cell interaction, and interfacial fluid dynamics involving Marangoni flow.SignificanceBacterial growth and pattern formation have strong bearing on their biological functions, such as their spread and accumulation, biofilm growth & its effects on infection and antibiotic resistance. The bacterial species of this study, Pseudomonas aeruginosa, is a human pathogen responsible for frequent infections in wounds, airways, and urinary tract, particularly when involving the use of catheters. The findings of this study and the mechanisms we propose offer new insights on the important behaviors of bacterial collective motility, pattern dynamics, and biofilm growth.

scholarly journals The Core Proteome of Biofilm-Grown Clinical Pseudomonas aeruginosa Isolates

Cells ◽  
2019 ◽  
Vol 8 (10) ◽  
pp. 1129 ◽  
Author(s):  
Jelena Erdmann ◽  
Janne G. Thöming ◽  
Sarah Pohl ◽  
Andreas Pich ◽  
Christof Lenz ◽  
...  
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Bacterial Species ◽  
Protein Profile ◽  
Opportunistic Pathogen ◽  
Growth Conditions ◽  
Protein Quantification ◽  
Clinical Isolates ◽  
Biofilm Growth ◽  
Regulatory Pathways ◽  
Data Independent Acquisition

Comparative genomics has greatly facilitated the identification of shared as well as unique features among individual cells or tissues, and thus offers the potential to find disease markers. While proteomics is recognized for its potential to generate quantitative maps of protein expression, comparative proteomics in bacteria has been largely restricted to the comparison of single cell lines or mutant strains. In this study, we used a data independent acquisition (DIA) technique, which enables global protein quantification of large sample cohorts, to record the proteome profiles of overall 27 whole genome sequenced and transcriptionally profiled clinical isolates of the opportunistic pathogen Pseudomonas aeruginosa. Analysis of the proteome profiles across the 27 clinical isolates grown under planktonic and biofilm growth conditions led to the identification of a core biofilm-associated protein profile. Furthermore, we found that protein-to-mRNA ratios between different P. aeruginosa strains are well correlated, indicating conserved patterns of post-transcriptional regulation. Uncovering core regulatory pathways, which drive biofilm formation and associated antibiotic tolerance in bacterial pathogens, promise to give clues to interactions between bacterial species and their environment and could provide useful targets for new clinical interventions to combat biofilm-associated infections.

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