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Bacterial flagella: twist and stick, or dodge across the kingdoms.

Rossez Y, Wolfson EB, Holmes A, Gally DL, Holden NJ - PLoS Pathog. (2015)

Bottom Line: An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components.At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms.These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

View Article: PubMed Central - PubMed

Affiliation: Cellular and Molecular Sciences, James Hutton Institute, Dundee, United Kingdom.

ABSTRACT
The flagellum organelle is an intricate multiprotein assembly best known for its rotational propulsion of bacteria. However, recent studies have expanded our knowledge of other functions in pathogenic contexts, particularly adherence and immune modulation, e.g., for Salmonella enterica, Campylobacter jejuni, Pseudomonas aeruginosa, and Escherichia coli. Flagella-mediated adherence is important in host colonisation for several plant and animal pathogens, but the specific interactions that promote flagella binding to such diverse host tissues has remained elusive. Recent work has shown that the organelles act like probes that find favourable surface topologies to initiate binding. An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components. At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms. Bacteria have evolved different strategies to evade or even promote this specific recognition, with some important differences shown for phytopathogens. These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

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The biophysical properties of flagella, to “twist and stick,” lend themselves towards nonspecific adhesion.Left, a summary of key characteristics of the flagella apparatus that are advantageous for adherence, and right, specific properties highlighted on the left. (A) Flagellum length results in a long reach towards colonization surfaces as an early-stage anchor—higher affinity binding can occur at closer proximity with specific adhesins and receptors. (B) Flagella rotation generates force that promotes membrane interactions during initial adherence. (C) Flagella are highly repetitive structures, non-specific low affinity binding can result in adhesion at high avidities.
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ppat.1004483.g001: The biophysical properties of flagella, to “twist and stick,” lend themselves towards nonspecific adhesion.Left, a summary of key characteristics of the flagella apparatus that are advantageous for adherence, and right, specific properties highlighted on the left. (A) Flagellum length results in a long reach towards colonization surfaces as an early-stage anchor—higher affinity binding can occur at closer proximity with specific adhesins and receptors. (B) Flagella rotation generates force that promotes membrane interactions during initial adherence. (C) Flagella are highly repetitive structures, non-specific low affinity binding can result in adhesion at high avidities.

Mentions: There is a large body of published work for flagella-mediated adherence, yet there are very few examples of specific interactions where both flagella and host determinants have been formally dissected. Instead, there is an emerging theme of nonspecific interactions, which has been challenging to investigate and likely relates to the biophysical properties of flagella (Fig. 1). Firstly, flagella organelles are long filaments that can reach up to 20 μm from the bacterial cell surface (Fig. 1A). It is therefore logical that flagella can be exploited as adhesive scaffolds and are involved in initial probing of surfaces as an early colonisation factor. Secondly, its motor can spin flagella filaments at speeds in excess of 15,000 rpm (Fig. 1B), which not only increases the chances of the filament coming into contact with surfaces, but also ensures it does so with force [8]. This is consistent with evidence that some flagella aren’t adhesive, but are involved in cellular binding and invasion in processes distinct from providing niche proximity through propulsion. In the absence of specific protein receptors, observation of intercalation and penetration into plant and animal membrane lipid layers by flagella could also be explained by this phenomenon. Thirdly, the flagellum filament is a polymeric structure, comprised of repeating epitopes of one or more flagellin types (Fig. 1C). Repeating epitopes are high avidity by definition: low affinity ionic interactions can be consolidated, amplified, and relevant if the binding substrate is also repetitive. With very few exceptions (innate immune receptors being the most notable), published examples of “specific” flagella binding interactions are with factors that are repetitive, such as polymeric proteins, proteoglycans, glycolipids, and phospholipids. Flagella therefore appear to be a tool with general properties that can be adapted to pathogenic colonisation of a diverse range of niches across plant and animal kingdoms.


Bacterial flagella: twist and stick, or dodge across the kingdoms.

Rossez Y, Wolfson EB, Holmes A, Gally DL, Holden NJ - PLoS Pathog. (2015)

The biophysical properties of flagella, to “twist and stick,” lend themselves towards nonspecific adhesion.Left, a summary of key characteristics of the flagella apparatus that are advantageous for adherence, and right, specific properties highlighted on the left. (A) Flagellum length results in a long reach towards colonization surfaces as an early-stage anchor—higher affinity binding can occur at closer proximity with specific adhesins and receptors. (B) Flagella rotation generates force that promotes membrane interactions during initial adherence. (C) Flagella are highly repetitive structures, non-specific low affinity binding can result in adhesion at high avidities.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4295861&req=5

ppat.1004483.g001: The biophysical properties of flagella, to “twist and stick,” lend themselves towards nonspecific adhesion.Left, a summary of key characteristics of the flagella apparatus that are advantageous for adherence, and right, specific properties highlighted on the left. (A) Flagellum length results in a long reach towards colonization surfaces as an early-stage anchor—higher affinity binding can occur at closer proximity with specific adhesins and receptors. (B) Flagella rotation generates force that promotes membrane interactions during initial adherence. (C) Flagella are highly repetitive structures, non-specific low affinity binding can result in adhesion at high avidities.
Mentions: There is a large body of published work for flagella-mediated adherence, yet there are very few examples of specific interactions where both flagella and host determinants have been formally dissected. Instead, there is an emerging theme of nonspecific interactions, which has been challenging to investigate and likely relates to the biophysical properties of flagella (Fig. 1). Firstly, flagella organelles are long filaments that can reach up to 20 μm from the bacterial cell surface (Fig. 1A). It is therefore logical that flagella can be exploited as adhesive scaffolds and are involved in initial probing of surfaces as an early colonisation factor. Secondly, its motor can spin flagella filaments at speeds in excess of 15,000 rpm (Fig. 1B), which not only increases the chances of the filament coming into contact with surfaces, but also ensures it does so with force [8]. This is consistent with evidence that some flagella aren’t adhesive, but are involved in cellular binding and invasion in processes distinct from providing niche proximity through propulsion. In the absence of specific protein receptors, observation of intercalation and penetration into plant and animal membrane lipid layers by flagella could also be explained by this phenomenon. Thirdly, the flagellum filament is a polymeric structure, comprised of repeating epitopes of one or more flagellin types (Fig. 1C). Repeating epitopes are high avidity by definition: low affinity ionic interactions can be consolidated, amplified, and relevant if the binding substrate is also repetitive. With very few exceptions (innate immune receptors being the most notable), published examples of “specific” flagella binding interactions are with factors that are repetitive, such as polymeric proteins, proteoglycans, glycolipids, and phospholipids. Flagella therefore appear to be a tool with general properties that can be adapted to pathogenic colonisation of a diverse range of niches across plant and animal kingdoms.

Bottom Line: An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components.At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms.These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

View Article: PubMed Central - PubMed

Affiliation: Cellular and Molecular Sciences, James Hutton Institute, Dundee, United Kingdom.

ABSTRACT
The flagellum organelle is an intricate multiprotein assembly best known for its rotational propulsion of bacteria. However, recent studies have expanded our knowledge of other functions in pathogenic contexts, particularly adherence and immune modulation, e.g., for Salmonella enterica, Campylobacter jejuni, Pseudomonas aeruginosa, and Escherichia coli. Flagella-mediated adherence is important in host colonisation for several plant and animal pathogens, but the specific interactions that promote flagella binding to such diverse host tissues has remained elusive. Recent work has shown that the organelles act like probes that find favourable surface topologies to initiate binding. An emerging theme is that more general properties, such as ionic charge of repetitive binding epitopes and rotational force, allow interactions with plasma membrane components. At the same time, flagellin monomers are important inducers of plant and animal innate immunity: variation in their recognition impacts the course and outcome of infections in hosts from both kingdoms. Bacteria have evolved different strategies to evade or even promote this specific recognition, with some important differences shown for phytopathogens. These studies have provided a wider appreciation of the functions of bacterial flagella in the context of both plant and animal reservoirs.

Show MeSH
Related in: MedlinePlus