Motility and Chemotaxis in Agrobacterium tumefaciens Surface Attachment and Biofilm Formation

Department of Biology, Indiana University, 1001 E. 3rd St., Jordan Hall 142, Bloomington, IN 47405-1847, USA.
Journal of bacteriology (Impact Factor: 2.81). 12/2007; 189(22):8005-14. DOI: 10.1128/JB.00566-07
Source: PubMed


Bacterial motility mechanisms, including swimming, swarming, and twitching, are known to have important roles in biofilm formation, including colonization and the subsequent expansion into mature structured surface communities. Directed motility requires chemotaxis functions that are conserved among many bacterial species. The biofilm-forming plant pathogen Agrobacterium tumefaciens drives swimming motility by utilizing a small group of flagella localized to a single pole or the subpolar region of the cell. There is no evidence for twitching or swarming motility in A. tumefaciens. Site-specific deletion mutations that resulted in either aflagellate, flagellated but nonmotile, or flagellated but nonchemotactic A. tumefaciens derivatives were examined for biofilm formation under static and flowing conditions. Nonmotile mutants were significantly deficient in biofilm formation under static conditions. Under flowing conditions, however, the aflagellate mutant rapidly formed aberrantly dense, tall biofilms. In contrast, a nonmotile mutant with unpowered flagella was clearly debilitated for biofilm formation relative to the wild type. A nontumbling chemotaxis mutant was only weakly affected with regard to biofilm formation under nonflowing conditions but was notably compromised in flow, generating less adherent biomass than the wild type, with a more dispersed cellular arrangement. Extragenic suppressor mutants of the chemotaxis-impaired, straight-swimming phenotype were readily isolated from motility agar plates. These mutants regained tumbling at a frequency similar to that of the wild type. Despite this phenotype, biofilm formation by the suppressor mutants in static cultures was significantly deficient. Under flowing conditions, a representative suppressor mutant manifested a phenotype similar to yet distinct from that of its nonchemotactic parent.

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    • "Chemotaxis is also relevant for plant pathogens. Chemotaxis is needed for the soil-borne plant pathogens Agrobacterium tumefa- ciens[41,42]and Ralstonia solanacearum[43,44]to find the correct host plant roots in their soil environments. Similarly, the plant leaf pathogen Pseudomonas syringae uses flagellar motility and chemotaxis for successful formation of infections on leaf surfaces[45]. "
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    ABSTRACT: The bacterial flagellum is an amazingly complex molecular machine with a diversity of roles in pathogenesis including reaching the optimal host site, colonization or invasion, maintenance at the infection site, and post-infection dispersal. Multi-megadalton flagellar motors self-assemble across the cell wall to form a reversible rotary motor that spins a helical propeller - the flagellum itself - to drive the motility of diverse bacterial pathogens. The flagellar motor responds to the chemoreceptor system to redirect swimming toward beneficial environments, thus enabling flagellated pathogens to seek out their site of infection. At their target site, additional roles of surface swimming and mechanosensing are mediated by flagella to trigger pathogenesis. Yet while these motility-related functions have long been recognized as virulence factors in bacteria, many bacteria have capitalized upon flagellar structure and function by adapting it to roles in other stages of the infection process. Once at their target site, the flagellum can assist adherence to surfaces, differentiation into biofilms, secretion of effector molecules, further penetration through tissue structures, or in activating phagocytosis to gain entry into eukaryotic cells. Next, upon onset of infection, flagellar expression must be adapted to deal with the host's immune system defenses, either by reduced or altered expression or by flagellar structural modification. Finally, after a successful growth phase on or inside a host, dispersal to new infection sites is often flagellar motility-mediated. Examining examples of all these processes from different bacterial pathogens, it quickly becomes clear that the flagellum is involved in bacterial pathogenesis for motility and a whole lot more.
    Full-text · Article · Nov 2015 · Seminars in Cell and Developmental Biology
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    • "In addition, many microbial taxa have evolved the ability to sense chemical gradients towards favorable conditions, moving towards gradients of attractants and away from gradients of repellents (Taylor and Stocker 2012; Stocker 2012). Cell motility (e.g., flagellum or chemotaxis mediated) was recognized to be linked to surface attachment and subsequent biofilm formation due to the increase in collision frequency (Morisaki et al. 1999; Merritt et al. 2007; Lemon et al. 2007). Nevertheless, understanding of the underlying mechanisms of disinfection-driven microbial attachment through cell motility regulation remains elusive. "
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    ABSTRACT: Microbial attachment to drinking water pipe surfaces facilitates pathogen survival and deteriorates disinfection performance, directly threatening the safety of drinking water. Notwithstanding that the formation of biofilm has been studied for decades, the underlying mechanisms for the origins of microbial surface attachment in biofilm development in drinking water pipelines remain largely elusive. We combined experimental and mathematical methods to investigate the role of environmental stress-mediated cell motility on microbial surface attachment in chlorination-stressed drinking water distribution systems. Results show that at low levels of disinfectant (0.0-1.0 mg/L), the presence of chlorine promotes initiation of microbial surface attachment, while higher amounts of disinfectant (>1.0 mg/L) inhibit microbial attachment. The proposed mathematical model further demonstrates that chlorination stress (0.0-5.0 mg/L)-mediated microbial cell motility regulates the frequency of cell-wall collision and thereby controls initial microbial surface attachment. The results reveal that transport processes and decay patterns of chlorine in drinking water pipelines regulate microbial cell motility and, thus, control initial surface cell attachment. It provides a mechanistic understanding of microbial attachment shaped by environmental disinfection stress and leads to new insights into microbial safety protocols in water distribution systems.
    Full-text · Article · Oct 2014 · Applied Microbiology and Biotechnology
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    • "These microbial biofilms form on natural and man-made surfaces and interfaces and play important roles in various health and environmental issues (Hall-Stoodley et al. 2004 ). Previous experimental studies have indicated the significance of bacterial motility mechanisms in the colonization process and the subsequent biofilm formation (O'Toole and Kolter 1998; Pratt and Kolter 1998; Watnick and Kolter 1999; Lemon et al. 2007; Merritt et al. 2007; Kim et al. 2008 ; Houry et al. 2010). In particular, flagellar mediated swimming is crucial in approaching the surface and initiating the adhesion process (Tuson and Weibel 2013) and pili-mediated motility highly promotes the surface exploration (Burrows 2012). "
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    ABSTRACT: We numerically study the effect of solid boundaries on the swimming behavior of a motile microorganism in viscoelastic media. Understanding the swimmer-wall hydrodynamic interactions is crucial to elucidate the adhesion of bacterial cells to nearby substrates which is precursor to the formation of the microbial biofilms. The microorganism is simulated using a squirmer model that captures the major swimming mechanisms of potential, extensile, and contractile types of swimmers, while neglecting the biological complexities. A Giesekus constitutive equation is utilized to describe both viscoelasticity and shear-thinning behavior of the background fluid. We found that the viscoelasticity strongly affects the near-wall motion of a squirmer by generating an opposing polymeric torque which impedes the rotation of the swimmer away from the wall. In particular, the time a neutral squirmer spends at the close proximity of the wall is shown to increase with polymer relaxation time and reaches a maximum at Weissenberg number of unity. The shear-thinning effect is found to weaken the solvent stress and therefore, increases the swimmer-wall contact time. For a puller swimmer, the polymer stretching mainly occurs around its lateral sides, leading to reduced elastic resistance against its locomotion. The neutral and puller swimmers eventually escape the wall attraction effect due to a releasing force generated by the Newtonian viscous stress. In contrast, the pusher is found to be perpetually trapped near the wall as a result of the formation of a highly stretched region behind its body. It is shown that the shear-thinning property of the fluid weakens the wall-trapping effect for the pusher squirmer.
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