Dataset Information

Reconstitution of a Biofilm Adhesin System from a Sulfate-Reducing Bacterium in Pseudomonas fluorescens.

ABSTRACT: Biofilms of the sulfate reducing bacterium (SRB) Desulfovibrio vulgaris Hildenborough (DvH) can facilitate metal corrosion in various industrial and environmental settings leading to substantial economic losses; however, the mechanisms of biofilm formation by DvH are not yet well-understood. Evidence suggests that a large adhesin, DvhA, may be contributing to biofilm formation in DvH. The dvhA gene and its neighbors encode proteins that resemble the Lap system, which regulates biofilm formation by Pseudomonas fluorescens, including a LapG-like protease DvhG and effector protein DvhD, which has key differences from the previously described LapD. By expressing the Lap-like adhesion components of DvH in P. fluorescens, our data support the model that the N-terminal fragment of the large adhesin DvhA serves as an adhesin "retention module" and is the target of the DvhG/DvhD regulatory module, thereby controlling cell-surface location of the adhesin. By heterologously expressing the DvhG/DvhD-like proteins in a P. fluorescens background lacking native regulation (ΔlapGΔlapD) we also show that cell surface regulation of the adhesin is dependent upon the intracellular levels of c-di-GMP. This study provides insight into the key players responsible for biofilm formation by DvH, thereby expanding our understanding of Lap-like systems.

SUBMITTER: Karbelkar AA

PROVIDER: S-EPMC10690286 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Reconstitution of a Biofilm Adhesin System from a Sulfate-Reducing Bacterium in Pseudomonas fluorescens.

Karbelkar Amruta A AA Font Maria E ME Smith T Jarrod TJ Sondermann Holger H O'Toole George A GA

bioRxiv : the preprint server for biology 20231122

Biofilms of the sulfate reducing bacterium (SRB) Desulfovibrio vulgaris Hildenborough (DvH) can facilitate metal corrosion in various industrial and environmental settings leading to substantial economic losses; however, the mechanisms of biofilm formation by DvH are not yet well-understood. Evidence suggests that a large adhesin, DvhA, may be contributing to biofilm formation in DvH. The dvhA gene and its neighbors encode proteins that resemble the Lap system, which regulates biof ...[more]

PMID: 38045380

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Project description:Mechanisms by which cells attach to a surface and form a biofilm are diverse and differ greatly among organisms. The Gram-negative gammaproteobacterium Pseudomonas fluorescens attaches to a surface through the localization of the large type 1-secreted RTX adhesin LapA to the outer surface of the cell. LapA localization to the cell surface is controlled by the activities of a periplasmic protease, LapG, and an inner membrane-spanning cyclic di-GMP-responsive effector protein, LapD. A previous study identified a second, LapA-like protein encoded in the P. fluorescens Pf0-1 genome: Pfl01_1463. Here, we identified specific growth conditions under which Pfl01_1463, here called MapA (medium adhesion protein A) is a functional adhesin contributing to biofilm formation. This adhesin, like LapA, appears to be secreted through a Lap-related type 1 secretion machinery, and its localization is controlled by LapD and LapG. However, differing roles of LapA and MapA in biofilm formation are achieved, at least in part, through the differences in the sequences of the two adhesins and different distributions of the expression of the lapA and mapA genes within a biofilm. LapA-like proteins are broadly distributed throughout the Proteobacteria, and furthermore, LapA and MapA are well conserved among other Pseudomonas species. Together, our data indicate that the mechanisms by which a cell forms a biofilm and the components of a biofilm matrix can differ depending on growth conditions and the matrix protein(s) expressed.IMPORTANCE Adhesins are critical for the formation and maturation of bacterial biofilms. We identify a second adhesin in P. fluorescens, called MapA, which appears to play a role in biofilm maturation and whose regulation is distinct from the previously reported LapA adhesin, which is critical for biofilm initiation. Analysis of bacterial adhesins shows that LapA-like and MapA-like adhesins are found broadly in pseudomonads and related organisms, indicating that the utilization of different suites of adhesins may be broadly important in the Gammaproteobacteria.

Project description:Sulfate-reducing bacteria (SRB) colonize the guts of ~50% of humans. We used genome-wide transposon mutagenesis and insertion-site sequencing (INSeq), RNA-Seq, plus mass spectrometry to characterize genetic and environmental factors that impact the niche of Desulfovibrio piger, the most common SRB in a surveyed cohort of healthy USA adults. Gnotobiotic mice were colonized with an assemblage of sequenced human gut bacterial species with or without D. piger and fed diets with different levels and types of carbohydrates and sulfur sources. Diet was a major determinant of functions expressed by this artificial 9-member community and of the genes that impact D. piger fitness; the latter includes high- and low-affinity systems for utilizing ammonia, a limiting resource for D. piger in mice consuming a polysaccharide-rich diet. While genes involved in hydrogen consumption and sulfate reduction are necessary for its colonization, varying dietary free sulfate levels did not significantly alter levels of D. piger, which can obtain sulfate from the host in part via cross-feeding mediated by Bacteroides-encoded sulfatases. Chondroitin sulfate, a common dietary supplement, increased D. piger and H2S levels without compromising gut barrier integrity. A chondroitin sulfate-supplemented diet together with D. piger impacted the assemblage’s substrate utilization preferences, allowing consumption of more reduced carbon sources, and increasing the abundance of the H2-producing Actinobacterium, Collinsella aerofaciens. Our findings provide genetic and metabolic details of how this H2-consuming SRB shapes the responses of a microbiota to diet ingredients, and a framework for examining how individuals lacking D. piger differ from those that harbor it. 8 samples total, 2 gropus of 4 mice: Proximal colon gene expression profiles of gnotobiotic mice colonized with an artificial gut community composed of 8 human gut species (group 1: NoDp) and from mice colonized with the same community plus D. piger (Dp). Mice were fed a HF/HS diet supplemented with 3% chondroitin sulfate. Animals were sacrificed 2 weeks after colonization

Dataset Information

Reconstitution of a Biofilm Adhesin System from a Sulfate-Reducing Bacterium in Pseudomonas fluorescens.

Publications

Reconstitution of a Biofilm Adhesin System from a Sulfate-Reducing Bacterium in <i>Pseudomonas fluorescens</i>.

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