Comparative Analysis of Ionic Strength Tolerance between Freshwater and Marine Caulobacterales Adhesins

Abstract

Bacterial adhesion is affected by environmental factors, such as ionic strength, pH, temperature, and shear forces. Therefore, marine bacteria must have developed adhesins with different compositions and structures than those of their freshwater counterparts to adapt to their natural environment. The dimorphic alphaproteobacterium Hirschia baltica is a marine budding bacterium in the clade Caulobacterales. H. baltica uses a polar adhesin, the holdfast, located at the cell pole opposite the reproductive stalk, for surface attachment and cell-cell adhesion. The holdfast adhesin has been best characterized in Caulobacter crescentus, a freshwater member of the Caulobacterales, and little is known about holdfast compositions and properties in marine Caulobacterales. Here, we use H. baltica as a model to characterize holdfast properties in marine Caulobacterales. We show that freshwater and marine Caulobacterales use similar genes in holdfast biogenesis and that these genes are highly conserved among the species in the two genera. We determine that H. baltica produces a larger holdfast than C. crescentus and that the holdfasts have different chemical compositions, as they contain N-acetylglucosamine and galactose monosaccharide residues and proteins but lack DNA. Finally, we show that H. baltica holdfasts tolerate higher ionic strength than those of C. crescentus. We conclude that marine Caulobacterales holdfasts have physicochemical properties that maximize binding in high-ionic-strength environments. IMPORTANCE Most bacteria spend a large part of their life spans attached to surfaces, forming complex multicellular communities called biofilms. Bacteria can colonize virtually any surface, and therefore, they have adapted to bind efficiently in very different environments. In this study, we compare the adhesive holdfasts produced by the freshwater bacterium C. crescentus and a relative, the marine bacterium H. baltica. We show that H. baltica holdfasts have a different morphology and chemical composition and tolerate high ionic strength. Our results show that the H. baltica holdfast is an excellent model to study the effect of ionic strength on adhesion and provides insights into the physicochemical properties required for adhesion in the marine environment.

Structural Diversity in Early-Stage Biofilm Formation on Microplastics Depends on Environmental Medium and Polymer Properties

“…It must be considered that beside the similar pH values of freshwater and seawater, the ionic strength may be different. Due to a higher amount of solved salts in seawater, the ionic strength is described to be 500 times higher than in freshwater [59]. As soon as the polymers face either freshwater or seawater, their surfaces may interact with available ions, influencing their ζ-potential immediately.…”

Substratum‐associated microbiota

“…Hentchel et al (2019) grew axenic cultures of C. crescentus in complex and chemically defined media to examine the fitness of transposon mutants in freshwater environments and described a new model system to study gene function in ecosystems. In a comparison of the physicochemical properties of adherence between freshwater and marine Caulobacterales, Chepkwony, Berne, and Brun (2019) found the marine Hirschia baltica maximized binding via their holdfast in environments with high ionic strength. Caulobacter crescentus shifts cell morphology in response to changing growth conditions (Heinrich, Leslie, Morlock, Bertilsson, & Jonas, 2019).…”

Ionic Strength-Dependent Attachment of Pseudomonas aeruginosa PAO1 on Graphene Oxide Surfaces

“…Previous atomic force microscopy (AFM)-based studies revealed that the bacteria–GO interaction was predominantly repulsive due to the electrostatic and steric repulsion between deprotonated carboxylate groups in GO and the negatively charged cell surface. , On the other hand, the enhanced bacterial attachment to GO-coated organic and inorganic surfaces via hydrophobic interaction has been demonstrated. − These contradictory conclusions are mainly derived from the various parameters influencing the interfacial behaviors. It has been recognized that the chemical properties of the background electrolyte such as ionic strength govern the extent and mechanisms of bacterial attachment to surfaces. − Moreover, the lack of real-time and quantitative analysis of the bacterial deposition dynamics on GO surface also leads to divergent results from different investigators. ,, As bacterial attachment onto GO is critical in determining GO’s antibiofouling and antibacterial performance, it is crucial to reveal the effect of solution chemistry on the dynamic bacterial attachment processes on GO surface and develop a comprehensive understanding of bacteria–GO interaction.…”