Pilus Production in Acinetobacter baumannii Is Growth Phase Dependent and Essential for Natural Transformation.

Melanie Blokesch,Nina Vesel,Thomas J Silhavy

doi:10.1128/jb.00034-21

Melanie Blokesch, Nina Vesel + Show 1 more

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https://doi.org/10.1128/jb.00034-21

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Abstract

Acinetobacter baumannii is a severe threat to human health as a frequently multidrug-resistant hospital-acquired pathogen. Part of the danger from this bacterium comes from its genome plasticity and ability to evolve quickly by taking up and recombining external DNA into its own genome in a process called natural competence for transformation. This mode of horizontal gene transfer is one of the major ways that bacteria can acquire new antimicrobial resistances and toxic traits. Because these processes in A. baumannii are not well studied, we herein characterized new aspects of natural transformability in this species that include the species' competence window. We uncovered a strong correlation with a growth phase-dependent synthesis of a type IV pilus (TFP), which constitutes the central part of competence-induced DNA uptake machinery. We used bacterial genetics and microscopy to demonstrate that the TFP is essential for the natural transformability and surface motility of A. baumannii, whereas pilus-unrelated proteins of the DNA uptake complex do not affect the motility phenotype. Furthermore, TFP biogenesis and assembly is subject to input from two regulatory systems that are homologous to Pseudomonas aeruginosa, namely, the PilSR two-component system and the Pil-Chp chemosensory system. We demonstrated that these systems affect not only the piliation status of cells but also their ability to take up DNA for transformation. Importantly, we report on discrepancies between TFP biogenesis and natural transformability within the same genus by comparing data for our work on A. baumannii to data reported for Acinetobacter baylyi, the latter of which served for decades as a model for natural competence.IMPORTANCE Rapid bacterial evolution has alarming negative impacts on animal and human health which can occur when pathogens acquire antimicrobial resistance traits. As a major cause of antibiotic-resistant opportunistic infections, A. baumannii is a high-priority health threat which has motivated renewed interest in studying how this pathogen acquires new, dangerous traits. In this study, we deciphered a specific time window in which these bacteria can acquire new DNA and correlated that with its ability to produce the external appendages that contribute to the DNA acquisition process. These cell appendages function doubly for motility on surfaces and for DNA uptake. Collectively, we showed that A. baumannii is similar in its TFP production to Pseudomonas aeruginosa, though it differs from the well-studied species A. baylyi.

Highlights

Bacterial evolution is a major human health concern, as it can lead to the acquisition of concerning traits, such as new antimicrobial resistances or virulence genes
We recently reported that such transformation events can lead to frequent exchanges of genomic regions greater than 100 kbp in the naturally competent bacterium Vibrio cholerae, which could explain how bacteria such as A. baumannii acquire new DNA stretches including resistances
A. baumannii’s dilution into fresh medium or upon entry into the stationary phase (Fig. 1). This behavior is distinct from A. baylyi, which can reach transformation frequencies up to 0.7% of all cells [43] and is transformable throughout all growth phases with varying efficiencies [44, 45]. This underscores the importance of studying A. baumannii in its own right and not relying on assumptions made from model bacteria

Summary

Introduction

Bacterial evolution is a major human health concern, as it can lead to the acquisition of concerning traits, such as new antimicrobial resistances or virulence genes. One pathogen of concern is the hospital-prevalent antimicrobial-resistant Acinetobacter baumannii [1, 2], which evolves rapidly by incorporating significant amounts of DNA from other organisms in a process called horizontal gene transfer (HGT) [3]. Using a type of HGT called natural competence for transformation, A. baumannii is able to take up extracellular DNA from its environment and incorporate it into its own genome by homologous recombination [4,5,6,7]. We recently reported that such transformation events can lead to frequent exchanges of genomic regions greater than 100 kbp in the naturally competent bacterium Vibrio cholerae, which could explain how bacteria such as A. baumannii acquire new DNA stretches including resistances. The few studies on transformation in A. baumannii have focused mainly on mild competence inducers such as serum albumin and Ca2+, on transforming materials, and the pH [10,11,12]

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