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Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability.

ABSTRACT: The structure of bacterial biofilms depends on environmental conditions, such as availability of nutrients, during biofilm formation. In turn, variations in biofilm structure in part reflect differences in bacterial motility during early biofilm formation. Pseudomonas aeruginosa deprived of nutrients remain dispersed on a surface, whereas cells supplemented with additional nutrients cluster and form microcolonies. At the single-cell scale, how bacteria modify their motility to favour distinct life cycle outcomes remains poorly understood. High-throughput algorithms were used to track thousands of P. aeruginosa moving using type-IV pili (TFP) on surfaces in varying nutrient conditions and hence identify four distinct motility types. A minimal stochastic model was used to reproduce the TFP-driven motility types. We report that P. aeruginosa cells differently deploy TFP to alter the distribution of motility types under different nutrient conditions. Bacteria preferentially crawl unidirectionally under nutrient-limited conditions, but preferentially stall under nutrient-supplemented conditions. Motility types correlate with subcellular localisation of FimX, a protein required for TFP assembly and implicated in environmental response. The subcellular distribution of FimX is asymmetric for unidirectional crawling, consistent with TFP assembled primarily at the leading pole, whereas for non-translational types FimX expression is symmetric or non-existent. These results are consistent with a minimal stochastic model that reproduces the motility types from the subcellular average concentration and asymmetry of FimX. These findings reveal that P. aeruginosa deploy TFP symmetrically or asymmetrically to modulate motility behaviours in different nutrient conditions and thereby form biofilms only where nutrients are sufficient, which greatly enhances their competitive capacity in diverse environments.

SUBMITTER: Ni L

PROVIDER: S-EPMC5515259 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability.

Ni Lei L Yang Shuai S Zhang Rongrong R Jin Zhenyu Z Chen Hao H Conrad Jacinta C JC Jin Fan F

NPJ biofilms and microbiomes 20160224

The structure of bacterial biofilms depends on environmental conditions, such as availability of nutrients, during biofilm formation. In turn, variations in biofilm structure in part reflect differences in bacterial motility during early biofilm formation. <i>Pseudomonas aeruginosa</i> deprived of nutrients remain dispersed on a surface, whereas cells supplemented with additional nutrients cluster and form microcolonies. At the single-cell scale, how bacteria modify their motility to favour dist ...[more]

PMID: 28721239

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Project description:BackgroundIn Gram-negative bacteria, type IV pili (TFP) have long been known to play important roles in such diverse biological phenomena as surface adhesion, motility, and DNA transfer, with significant consequences for pathogenicity. More recently it became apparent that Gram-positive bacteria also express type IV pili; however, little is known about the diversity and abundance of these structures in Gram-positives. Computational tools for automated identification of type IV pilins are not currently available.ResultsTo assess TFP diversity in Gram-positive bacteria and facilitate pilin identification, we compiled a comprehensive list of putative Gram-positive pilins encoded by operons containing highly conserved pilus biosynthetic genes (pilB, pilC). A surprisingly large number of species were found to contain multiple TFP operons (pil, com and/or tad). The N-terminal sequences of predicted pilins were exploited to develop PilFind, a rule-based algorithm for genome-wide identification of otherwise poorly conserved type IV pilins in any species, regardless of their association with TFP biosynthetic operons (http://signalfind.org). Using PilFind to scan 53 Gram-positive genomes (encoding >187,000 proteins), we identified 286 candidate pilins, including 214 in operons containing TFP biosynthetic genes (TBG+ operons). Although trained on Gram-positive pilins, PilFind identified 55 of 58 manually curated Gram-negative pilins in TBG+ operons, as well as 53 additional pilin candidates in operons lacking biosynthetic genes in ten species (>38,000 proteins), including 27 of 29 experimentally verified pilins. False positive rates appear to be low, as PilFind predicted only four pilin candidates in eleven bacterial species (>13,000 proteins) lacking TFP biosynthetic genes.ConclusionsWe have shown that Gram-positive bacteria contain a highly diverse set of type IV pili. PilFind can be an invaluable tool to study bacterial cellular processes known to involve type IV pilus-like structures. Its use in combination with other currently available computational tools should improve the accuracy of predicting the subcellular localization of bacterial proteins.

Project description:Drosophila melanogaster gut microbes play important roles in host nutritional physiology. However, these associations are often indirect, and studies typically are in the context of specialized nutritional conditions, making it difficult to discern how microbiome-mediated impacts translate to physiologically relevant conditions, in the laboratory or nature. In this study, we quantified changes in dietary nutrients due to D. melanogaster gut bacteria on three artificial diets and a natural diet of grapes. We show that under all four diet conditions, bacteria altered the protein, carbohydrates, and moisture of the food substrate. An in-depth analysis of one diet revealed that bacteria also increased the levels of tryptophan, an essential amino acid encountered scarcely in nature. These nutrient changes result in an increased protein-to-carbohydrate (P:C) ratio in all diets, which we hypothesized to be a significant determinant of microbiome-mediated host nutritional physiology. To test this, we compared life history traits of axenic flies reared on the three artificial diets with increased P:C ratios or continuous bacterial inoculation. We found that while on some diets, an environment of nutritional plenitude had impacts on life history, it did not fully explain all microbiome-associated phenotypes. This suggests that other factors, such as micronutrients and feeding behavior, likely also contribute to life history traits in a diet-dependent manner. Thus, while some bacterial impacts on nutrition occur across diets, others are dictated by unique dietary environments, highlighting the importance of diet-microbiome interactions in D. melanogaster nutritional physiology.IMPORTANCE Both in the laboratory and in nature, D. melanogaster-associated microbes serve as nutritional effectors, either through the production of metabolites or as direct sources of protein biomass. The relationship between the microbiome and the resulting host nutritional physiology is significantly impacted by diet composition, yet studies involving D. melanogaster are performed using a wide range of artificial diets, making it difficult to discern which aspects of host-microbe interactions may be universal or diet dependent. In this study, we utilized three standard D. melanogaster diets and a natural grape diet to form a comprehensive understanding of the quantifiable nutritional changes mediated by the host microbial community. We then altered these artificial diets based on the observed microbe-mediated changes to demonstrate their potential to influence host physiology, allowing us to identify nutritional factors whose effects were either universal for the three artificial diets or dependent on host diet composition.

Project description:The rare actinomycete Actinoplanes missouriensis produces terminal sporangia containing a few hundred flagellated spores. After release from the sporangia, the spores swim rapidly in aquatic environments as zoospores. The zoospores stop swimming and begin to germinate in niches for vegetative growth. Here, we report the characterization and functional analysis of zoospore type IV pili in A. missouriensis The pilus gene (pil) cluster, consisting of three apparently ?FliA-dependent transcriptional units, is activated during sporangium formation similarly to the flagellar gene cluster, indicating that the zoospore has not only flagella but also pili. With a new method in which zoospores were fixed with glutaraldehyde to prevent pilus retraction, zoospore pili were observed relatively easily using transmission electron microscopy, showing 6?±?3 pili per zoospore (n?=?37 piliated zoospores) and a length of 0.62?±?0.35??m (n?=?206), via observation of fliC-deleted, nonflagellated zoospores. No pili were observed in the zoospores of a prepilin-encoding pilA deletion (?pilA) mutant. In addition, the deletion of pilT, which encodes an ATPase predicted to be involved in pilus retraction, substantially reduced the frequency of pilus retraction. Several adhesion experiments using wild-type and ?pilA zoospores indicated that the zoospore pili are required for the sufficient adhesion of zoospores to hydrophobic solid surfaces. Many zoospore-forming rare actinomycetes conserve the pil cluster, which indicates that the zoospore pili yield an evolutionary benefit in the adhesion of zoospores to hydrophobic materials as footholds for germination in their mycelial growth.IMPORTANCE Bacterial zoospores are interesting cells in that their physiological state changes dynamically: they are dormant in sporangia, show temporary mobility after awakening, and finally stop swimming to germinate in niches for vegetative growth. However, the cellular biology of a zoospore remains largely unknown. This study describes unprecedented zoospore type IV pili in the rare actinomycete Actinoplanes missouriensis Similar to the case for the usual bacterial type IV pili, zoospore pili appeared to be retractable. Our findings that the zoospore pili have a functional role in the adhesion of zoospores to hydrophobic solid surfaces and that the zoospores use both pili and flagella properly according to their different purposes provide an important insight into the cellular biology of the zoospore.

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Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability.

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Bacteria differently deploy type-IV pili on surfaces to adapt to nutrient availability.

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