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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    • "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.
    Applied Microbiology and Biotechnology 10/2014; 99(6). DOI:10.1007/s00253-014-6166-9 · 3.34 Impact Factor
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    • "May 2014 | Volume 5 | Article 176 | 3 biofilm formation (Merritt et al., 2007). Ectopic expression of a plasmid-borne wild-type cheA allele enhanced motility in swim agar but did not correct the attachment deficiency. "
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    ABSTRACT: For many pathogenic bacteria surface attachment is a required first step during host interactions. Attachment can proceed to invasion of host tissue or cells or to establishment of a multicellular bacterial community known as a biofilm. The transition from a unicellular, often motile, state to a sessile, multicellular, biofilm-associated state is one of the most important developmental decisions for bacteria. Agrobacterium tumefaciens genetically transforms plant cells by transfer and integration of a segment of plasmid-encoded transferred DNA (T-DNA) into the host genome, and has also been a valuable tool for plant geneticists. A. tumefaciens attaches to and forms a complex biofilm on a variety of biotic and abiotic substrates in vitro. Although rarely studied in situ, it is hypothesized that the biofilm state plays an important functional role in the ecology of this organism. Surface attachment, motility, and cell division are coordinated through a complex regulatory network that imparts an unexpected asymmetry to the A. tumefaciens life cycle. In this review, we describe the mechanisms by which A. tumefaciens associates with surfaces, and regulation of this process. We focus on the transition between flagellar-based motility and surface attachment, and on the composition, production, and secretion of multiple extracellular components that contribute to the biofilm matrix. Biofilm formation by A. tumefaciens is linked with virulence both mechanistically and through shared regulatory molecules. We detail our current understanding of these and other regulatory schemes, as well as the internal and external (environmental) cues mediating development of the biofilm state, including the second messenger cyclic-di-GMP, nutrient levels, and the role of the plant host in influencing attachment and biofilm formation. A. tumefaciens is an important model system contributing to our understanding of developmental transitions, bacterial cell biology, and biofilm formation.
    Frontiers in Plant Science 05/2014; 5:176. DOI:10.3389/fpls.2014.00176 · 3.95 Impact Factor
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    • "The impact of chemotaxis in biofilm development depends on the bacterial species. Some works show a direct relationship between chemotaxis, attachment and biofilm development in Agrobacterium tumefaciens (Merritt et al., 2007) and Pseudomonas aeruginosa (Schmidt et al., 2011). However, in E. coli, chemotaxis was described as a non-critical process for a normal biofilm formation (Pratt & Kolter, 1998). "
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    ABSTRACT: Xanthomonas citri spp. citri (Xcc)develops a biofilm structure both in vitro and in vivo. Despite all the progress achieved by studies regarding biofilm formation, many of its mechanisms remain poorly understood. This work focuses on the identification of new genes involved in biofilm formation and how they are related to motility, virulence and chemotaxis in Xcc. A Tn5 library of approximately 6,000 Xcc (strain 306) mutants was generated and screened to search for biofilm formation defective strains. We identified 23 genes whose association with the biofilm formation resulted in a novelty. The analysis of the 23 mutants revealed not only the involvement of new genes in biofilm formation but also reinforced the importance of exopolysaccharide production, motility and cell surface structures in this process. This collection of biofilm defective mutants underscores the multifactorial genetic program underlying the establishment of biofilm in Xcc.
    Microbiology 06/2013; 159(Pt_9). DOI:10.1099/mic.0.064709-0 · 2.56 Impact Factor
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