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Claessen, D.

Publications and source records attributed to Claessen, D..

At least 19 recordsLinked to original sources

Fluorescence-activated cell sorting of Escherichia coli L-forms reveals maintained synchronized nucleic acid synthesis dynamics

L-form bacteria are wall-deficient variants that proliferate without an intact cell wall and independently of the canonical cell division machinery. Despite increasing insights into how L-forms survive and proliferate without a cell wall, fundamental questions regarding how cell cycle processes, including DNA and RNA synthesis, are coordinated in the wall-less state remain poorly understood. Here, we demonstrate that fluorescence-activated cell sorting (FACS) provides a robust approach for quantitative analysis of Escherichia coli L-forms. Flow cytometry revealed two reversible subpopulations differing in intracellular nucleic acid content, which rapidly re-established their heterogeneous distribution following sorting. Remarkably, cells with initially low nucleic acid content underwent a synchronized, population-wide increase in nucleic acid synthesis within 24 hours, a phenomenon that was independently confirmed by time-lapse fluorescence microscopy. Analysis of liquid cultures stained with SYTO and DAPI dyes showed that this transient increase occurred during early exponential growth and was driven predominantly by RNA rather than DNA synthesis. Consistent with observations in walled E. coli, RNA levels peaked before declining as cultures transitioned towards nutrient limitation. Together, these findings establish FACS as a powerful tool for studying L-form biology and reveal that, despite the absence of an intact cell wall and canonical cell division, L-forms retain coordinated, population-wide regulation of nucleic acid synthesis.

microbiology↗

Defining the minimal structural requirements of DivIVA in filamentous Actinomycetota

The morphogenetic protein DivIVA exhibits diverse functions across bacterial phyla. In Bacillota, DivIVA is primarily involved in cell division, whereas in Actinomycetota, it plays a central role in coordinating polar growth. Due to its essential nature, gaining insight into DivIVA function is challenging. Here we report on the functionality of truncated DivIVA proteins, using a unique divIVA deletion mutant created in cell wall-deficient Kitasatospora viridifaciens L-forms. DivIVA comprises an N-terminal domain, two coiled-coil regions separated by an intercoil linker, and a C-terminal domain. Deleting either the intercoil or the C-terminal region impacted branching dynamics. We also created a minimized variant wherein both were deleted simultaneously, containing the N-terminus and fused coiled-coils, resembling DivIVA from unicellular bacteria. Expression of this minimized variant resulted in severe growth defects. Cells exhibited a strong increase in hyphal width and cell wall thickness, accompanied by frequent tip bursting. Finally, we successfully introduced chimeric DivIVA from the unicellular actinobacterium Mycolicibacterium smegmatis with an N-terminal domain of Kitasatospora viridifaciens, demonstrating functional conservation within the phylum. In contrast, a chimeric DivIVA from Bacillus subtilis could not support growth, underscoring that polar growth is encoded within Actinomycetota-specific amino acid motifs encoded in the first and second coiled-coil. These findings enhance our understanding of the structure-function relationship for DivIVA and present new opportunities to study polar growth. ImpactDivIVA is essential for polar growth in Actinomycetota. In Streptomycetaceae, this membrane-binding protein localizes at growing hyphal tips and along lateral hyphal walls where new branches emerge. Due to its essentiality, the structural relationship of DivIVA between unicellular and multicellular species remains elusive. Using a Kitasatospora viridifaciens L-form divIVA deletion mutant, we expressed truncated DivIVA variants to identify essential regions. Deleting two large unstructured domains produced a minimized variant containing the N-terminus and fused coiled-coils, resembling DivIVA from unicellular bacteria. This strongly impacted morphogenesis, increasing hyphal width and cell wall thickness, and leading to hyphal tip bursting. Finally, we successfully substituted DivIVA of K. viridifaciens with that from Mycolicibacterium smegmatis. Furthermore, Bacillus subtilis DivIVA could not facilitate reversion, showing that polar growth depends on amino acid motifs unique to Actinomycetota. These findings enhance our understanding of the structure-function relationship of DivIVA and offer new opportunities to study polar growth.

microbiology↗

Enhanced extracellular matrix production provides protection to cell wall-deficient Escherichia coli

Escherichia coli-induced recurrent urinary tract infections (rUTIs) present a complicated challenge within the medical field. Most first-line antibiotic treatments primarily target cell-wall synthesis, which can lead to the formation of cell wall-deficient cells. To investigate how such cells can sustain, we obtained an E. coli strain capable of efficiently proliferating without its cell wall. One of the mutations lead to enhanced expression of rcsA, encoding an important regulator involved in responding to cell envelope stress. RNA sequencing demonstrated an upregulation of genes associated with the production of extracellular matrix components, and this increased extracellular matrix production was confirmed using various imaging techniques. Remarkably, a subsequent long-term evolution experiment on this strain revealed a further augmentation in extracellular matrix production, coinciding with an enhanced ability to withstand harsh conditions. These findings demonstrate how E. coli adapts to loss of its cell wall and that an increased synthesis of matrix constituents can compensate for the protective properties of the cell wall. SignificanceThe cell envelope is crucial for the protection of E. coli. During bacterial infections such as urinary tract infections, antibiotics that disrupt cell wall synthesis are commonly prescribed. However, this can stimulate the formation of wall-deficient bacteria that are still able to proliferate despite the presence of these drugs. Our findings reveal that loss of the cell wall in E. coli increases the production of extracellular matrix, a mechanism found in other unicellular organism too. This adaptation allows the bacteria to maintain their structural integrity and survive, highlighting a potential challenge in the successful treatment of bacterial infections.

microbiology↗

A family of lanthipeptides with anti-phage function

Bacteria synthesize natural products to adapt to their environment, where phage-bacteria interactions play a crucial role in bacterial ecology. Although a few natural products have been shown to protect bacteria from phage infection, the prevalence and diversity of chemical anti-phage defense remain largely unexplored. Here, we uncover a novel family of over 2000 lanthipeptide biosynthetic gene clusters from Actinobacteria that participate in anti-phage defense, which we named lanthiphages. Lanthiphages colocalize with other anti-phage systems in defense islands. We demonstrate that native lanthiphage expression protects the model strain Streptomyces coelicolor against diverse phages. Heterologous expression of four additional lanthiphage pathways shows that the anti-phage function is conserved across this family of biosynthetic gene clusters. Finally, we demonstrate that lanthiphage expression leads to the production of a novel compound and alters phage transcription. Our findings highlight that biosynthetic gene clusters with anti-phage functions can be successfully identified through genomic analysis. This work paves the way for the systematic mining of anti-phage natural products, which could constitute a novel reservoir of antiviral drugs.

microbiology↗

Bacterial heterozygosity promotes survival under multidrug selection

Although bacterial cells typically contain a single chromosome, some species are naturally polyploid and carry multiple copies of their chromosome. Polyploid chromosomes can be identical or heterogeneous, the latter giving rise to bacterial heterozygosity. While the benefits of heterozygosity are well studied in eukaryotes, its consequences in bacteria are unknown. Here we examine this question in the context of antibiotic resistance to understand how bacterial heterozygosity affects bacterial survival. Using a cell wall deficient model system in the actinomycete Kitasatospora viridifaciens, we found that heterozygous cells containing different chromosomes expressing different antibiotic resistance markers persist across a broader range of antibiotic concentrations. Recombinant cells containing the same resistance genes on a single chromosome also survive these conditions, but these cells pay a significant fitness cost due to constitutive expression of these genes. By contrast, heterozygous cells mitigate these costs by flexibly adjusting the ratio of their different chromosomes, thereby allowing rapid responses in temporally and spatially variable environments. Our results provide evidence that bacterial heterozygosity can increase adaptive plasticity in bacterial cells, in a similar manner to the evolutionary benefits provided by multicopy plasmids in bacteria. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=104 SRC="FIGDIR/small/593358v1_ufig1.gif" ALT="Figure 1"> View larger version (43K): org.highwire.dtl.DTLVardef@b7a6e8org.highwire.dtl.DTLVardef@12edf40org.highwire.dtl.DTLVardef@4323fborg.highwire.dtl.DTLVardef@1ef6416_HPS_FORMAT_FIGEXP M_FIG C_FIG O_LIHeterozygotic bacterial cells (polyploid with multiple chromosome types) can persist across a wider range of conditions than homozygotic cells. C_LIO_LIHeterozygous cells can adaptively adjust chromosomal frequencies in response to external conditions C_LIO_LIFlexibly adjusting chromosome ratios enables heterozygous cells to mitigate the costs of antibiotic resistance and allows rapid responses to temporally and spatially variable environments C_LIO_LIHeterozygosity can increase adaptive plasticity in bacterial cells, in a similar manner to the evolutionary benefits provided by multicopy plasmids. C_LI

microbiology↗

CslA and GlxA from Streptomyces lividans form a functional cellulose synthase complex

Filamentous growth of streptomycetes coincides with the synthesis and deposition of an uncharacterized protective glucan at hyphal tips. Synthesis of this glucan depends on the integral membrane protein CslA and the radical copper oxidase GlxA, which are part of a presumably large multiprotein complex operating at growing tips. Here, we show that CslA and GlxA interact by forming a protein complex that is sufficient to synthesize cellulose in vitro. Mass spectrometry analysis revealed that the purified complex produces cellulose chains with a degree of polymerization of at least 80 residues. Truncation analyses demonstrated that the removal of a significant extracellular segment of GlxA had no impact on complex formation, but significantly diminished activity of CslA. Altogether, our work demonstrates that CslA and GlxA form the active core of the cellulose synthase complex and provides molecular insights into a unique cellulose biosynthesis system that is conserved in streptomycetes. SignificanceCellulose stands out as the most abundant polysaccharide on Earth. While the synthesis of this polysaccharide has been extensively studied in plants and Gram-negative bacteria, the mechanisms in Gram-positive bacteria have remained largely unknown. Our research unveils a novel cellulose synthase complex formed by the interaction between the cellulose synthase-like protein CslA and the radical copper oxidase GlxA from Streptomyces lividans, a soil-dwelling Gram-positive bacterium. This discovery provides molecular insights into the distinctive cellulose biosynthesis machineries. Beyond expanding our understanding of cellulose biosynthesis, this study also opens avenues for exploring biotechnological applications and ecological roles of cellulose in Gram-positive bacteria, thereby contributing to the broader field of microbial cellulose biosynthesis and biofilm research.

microbiology↗

Mycobacteria form viable cell wall-deficient cells that are undetectable by conventional diagnostics

The cell wall is a unifying trait in bacteria and provides protection against environmental insults. Therefore, the wall is considered essential for most bacteria. Despite this critical role, many bacteria can transiently shed their cell wall and recent observations suggest a link of such wall-deficient cells to chronic infections. Whether shedding the cell wall also occurs in mycobacteria has not been established unambiguously. Here we provide compelling evidence that a wide range of mycobacterial species, including clinical and non-clinical isolates, form viable cell wall-deficient cells in response to environmental stressors. Using cryo-transmission electron micrography we show that the complex multi-layered wall is largely lost in such cells. Notably, we show that their formation in Mycobacterium marinum and BCG vaccine strains of Mycobacterium bovis is stimulated by exposure to cell wall-targeting antibiotics. Given that these wall-deficient mycobacteria are undetectable using conventional diagnostic methods, such cells have likely been overlooked in clinical settings. Altogether, these results indicate that mycobacteria can readily switch between a walled and wall-deficient lifestyle, which provides a plausible explanation for enabling persistence of infections caused by members of this genus.

microbiology↗

Reproducible switching between a walled and cell wall-deficient lifestyle of actinomycetes using gradient agar plates

The cell wall is a shape-defining structure that envelopes almost all bacteria, protecting them from biotic and abiotic stresses. Paradoxically, some filamentous actinomycetes have a natural ability to shed their cell wall under influence of hyperosmotic stress. These wall-deficient cells can revert to their walled state when transferred to a medium without osmoprotection but often lyse due to their fragile nature. Here, we designed plates with an osmolyte gradient to reduce cell lysis and thereby facilitating the transition between a walled and wall-deficient state. These gradient plates allow determining of the osmolyte concentration where switching takes place, thereby enabling careful and reproducible comparison between mutants affected by switching. Exploring these transitions could give valuable insights into the ecology of actinomycetes and their biotechnological applications. HIGHLIGHTS- Using agar plates with a gradient of osmoprotectants, revertant Streptomycetes can gradually revert to a walled state, thereby dramatically decreasing lysis. - Our method allows precise determination of the osmolyte concentration where reversion takes place, allowing careful and reproducible comparison between mutants. - Gradient agar plates can also be used to study chemical differentiation in Streptomycetes as a response to osmotic stress.

microbiology↗

A flexible and efficient microfluidics platform for the characterization and isolation of novel bacteriophages

Bacteriophages are viruses that infect bacteria. This property makes them highly suitable for varied uses in industry or in the development of the treatment of bacterial infections. However, the conventional methods that are used to isolate and analyze these bacteriophages from the environment are generally cumbersome and time-consuming. Here, we adapted a high-throughput microfluidic setup for long-term analysis of bacteriophage-bacteria interaction and demonstrate isolation of phages from environmental samples.

microbiology↗

DNA uptake by cell wall-deficient bacteria reveals a putative ancient macromolecule uptake mechanism

Horizontal gene transfer in bacteria is widely believed to occur via three main mechanisms: conjugation, transduction and transformation. These mechanisms facilitate the passage of DNA across the protective cell wall using sophisticated machinery. We present here a new mechanism of DNA uptake that is independent of canonical DNA uptake machineries and is used by bacteria that live without a cell wall. We show that the cell wall-deficient bacteria engulf extracellular material, whereby intracellular vesicles are formed, and DNA is internalized. This mechanism is not specific to DNA, and allows uptake of other macromolecules and even 125 nm lipid nanoparticles (LNPs). Uptake was prevented by molecules known to inhibit eukaryotic endocytosis, suggesting this to be an energy-dependent process. Given that cell wall-deficient bacteria are considered a model for early life forms, our work provides a possible mechanism for primordial cells to acquire new genetic material or food before invention of the bacterial cell wall.

microbiology↗

Reversible bacteriophage resistance by shedding the bacterial cell wall

Phages are highly abundant in the environment and a major threat for bacteria. Therefore, bacteria have evolved sophisticated defense systems to withstand phage attacks. Here, we describe a previously unknown mechanism by which mono- and diderm bacteria survive infection with diverse lytic phages. Phage exposure leads to a rapid and near complete conversion of walled cells to a cell wall-deficient state, which remain viable in osmoprotective conditions and can revert to the walled state. While shedding the cell wall dramatically reduces the number of progeny phages produced by the host, it does not always preclude phage infection. Altogether, these results show that the formation of cell wall-deficient cells prevents complete eradication of the bacterial population and suggest that cell wall-deficiency may limit the efficacy of phage therapy, especially in highly osmotic environments or when used together with antibiotics that target the cell wall.

microbiology↗

Role for a lytic polysaccharide monooxygenase in cell wall remodelling

Peptidoglycan is a major constituent of the bacterial cell wall and an important determinant for providing protection to cells. Besides peptidoglycan (PG), many bacteria synthesize other glycans that become part of the cell wall. Streptomycetes grow apically, where they synthesize a glycan that is exposed at the outer surface, but how it gets there is unknown. Here we show that deposition of the apical glycan at the cell surface depends on two key enzymes, the endoglucanase CslZ and the lytic polysaccharide monooxygenase LpmP. Activity of these enzymes allows localized remodeling and degradation of the PG, and we propose that this facilitates passage of the glycan. The absence of both enzymes not only prevents morphological development, but also sensitizes strains to lysozyme. Given that lytic polysaccharide monooxygenases are commonly found in microbes, this newly identified biological role in cell-wall remodelling may be widespread.

microbiology↗

Generating heterokaryotic cells via bacterial cell-cell fusion

Cell-cell fusion is fundamentally important for tissue repair, virus transmission, and genetic recombination, among other functions. Fusion has been mainly studied in eukaryotic cells and lipid vesicles, while cell-cell fusion in bacteria is less well characterized, due to the cell wall acting as a fusion-limiting barrier. Here we use cell wall-deficient bacteria to investigate the dynamics of cell fusion in bacteria that replicate without their cell wall. Stable, replicating cells containing differently labeled chromosomes were successfully obtained from fusion. We find that the rate of cell-cell fusion depends on the fluidity of cell membranes. Furthermore, we show that not only the efficiency but also the specificity of cell-cell fusion can be controlled via a pair of synthetic membrane-associated lipopeptides. Our results provide a molecular handle to understand and control cell-cell fusion to generate heterokaryotic cells, which was an important step in the evolution of protocells and of increasing importance for the design of synthetic cells.

microbiology↗

Branching of sporogenic aerial hyphae in sflA and sflB mutants of Streptomyces coelicolor correlates to ectopic localization of DivIVA and FtsZ in time and space

Bacterial cytokinesis starts with the polymerization of the tubulin-like FtsZ, which forms the cell division scaffold. SepF aligns FtsZ polymers and also acts as a membrane anchor for the Z-ring. While in most bacteria cell division takes place at midcell, during sporulation of Streptomyces many septa are laid down almost simultaneously in multinucleoid aerial hyphae. The genomes of streptomycetes encode two additional SepF paralogs, SflA and SflB, which can interact with SepF. Here we show that the sporogenic aerial hyphae of sflA and sflB mutants of Streptomyces coelicolor frequently branch, a phenomenon never seen in the wild-type strain. The branching coincided with ectopic localization of DivIVA along the lateral wall of sporulating aerial hyphae. Constitutive expression of SflA and SflB largely inhibited hyphal growth, further correlating SflAB activity to that of DivIVA. SflAB localized in foci prior to and after the time of sporulation-specific cell division, while SepF co-localized with active septum synthesis. Foci of FtsZ and DivIVA frequently persisted between adjacent spores in spore chains of sflA and sflB mutants, at sites occupied by SflAB in wild-type cells. This may be caused by the persistance of SepF multimers in the absence of SflAB. Taken together, our data show that SflA and SflB play an important role in the control of growth and cell division during Streptomyces development.

microbiology↗

Mutational meltdown of microbial altruists in Streptomyces coelicolor colonies

In colonies of the filamentous multicellular bacterium Streptomyces coelicolor, a sub-population of cells arise that hyper-produce metabolically costly antibiotics, resulting in division of labor that maximizes colony fitness. Because these cells contain large genomic deletions that cause massive reductions to individual fitness, their behavior is altruistic, much like worker castes in social insects or somatic cells in multicellular organisms. To understand the reproductive and genomic fate of these mutant cells after their emergence, we use experimental evolution by serially transferring populations via spore-to-spore transfer for 25 cycles, reflective of the natural mode of bottlenecked transmission for these spore-forming bacteria. We show that, in contrast to wild-type cells, altruistic mutant cells continue to significantly decline in fitness during transfer while they delete larger and larger fragments from their chromosome ends. In addition, altruistic mutants acquire a roughly 10-fold increase in their base-substitution rates possibly due to mutations in genes for DNA replication and repair. Ecological damage, caused by reduced sporulation, coupled with irreversible DNA damage due to point mutations and deletions, leads to an inevitable and irreversible type of mutational meltdown in these cells. Taken together, these results suggest that the altruistic cells arising in this division of labor are analogous to reproductively sterile castes of social insects.

evolutionary biology↗

Rapidemic, a versatile and label-free DNAzyme-based platform for visual nucleic acid detection

In the last three decades, there have been recurring outbreaks of infectious diseases, brought to light with the recent outbreak of coronavirus disease 2019 (COVID-19). Attempts to effectively contain the spread of infectious diseases have been hampered by the lack of rapidly adaptable, accurate, and accessible point-of-care diagnostic testing. In this study, we present a novel design of a label-free DNAzyme-based detection method called Rapidemic. This assay combines recombinase polymerase amplification (RPA) with linear strand-displacement amplification (LSDA) and guanine-quadruplex (GQ) DNAzyme-catalysed colour-changing reaction. The colorimetry basis of the signal readout omits the need for extensive instrumentation. Moreover, the primer-based sequence detection of RPA gives Rapidemic a potential to be rapidly adapted to target a new sequence. As a proof of concept, we developed the assay to detect isolated genomic DNA of Saccharomyces cerevisiae. The use of low-pH buffers and the optimization of the dilution rates from each preceding reaction to the next showed to be successful strategies to enable visible detection with this method. These findings demonstrate for the first time that a label-free DNAzyme-based detection method can be coupled to RPA and LSDA for nucleic acid detection.

molecular biology↗

A novel and conserved cell wall enzyme that can substitute for the Lipid II synthase MurG

The cell wall is a stress-bearing structure and a unifying trait in bacteria. Without exception, synthesis of the cell wall involves formation of the precursor molecule Lipid II by the activity of the essential biosynthetic enzyme MurG, which is encoded in the division and cell wall synthesis (dcw) gene cluster. Here we present the discovery of a novel cell wall enzyme that can substitute for MurG. A mutant of Kitasatospora viridifaciens lacking a significant part of the dcw cluster including murG surprisingly produced Lipid II and wild-type peptidoglycan. Genomic analysis identified a distant murG paralogue, which encodes a putative enzyme that shares only around 31% aa sequence identity with MurG. We show that this enzyme can replace the canonical MurG, and we therefore designated it MurG2. Orthologues of murG2 are present in 38% of all genomes of Kitasatosporae and members of the sister genus Streptomyces. CRISPRi experiments showed that K. viridifaciens murG2 can also functionally replace murG in Streptomyces coelicolor, thus validating its bioactivity and demonstrating that it is active in multiple genera. Altogether, these results identify MurG2 as a bona fide Lipid II synthase, thus demonstrating plasticity in cell wall synthesis.

microbiology↗

Microbial piggy-back: how Streptomyces spores are transported by motile soil bacteria

Streptomycetes are sessile, soil-dwelling bacteria that produce diverse metabolites that impact plant health and the behavior of microbial communities. Emerging studies have demonstrated that Streptomyces spores are distributed through a variety of mechanisms, but it remains unclear how spores are transported to their preferred micro-environments, such as plant roots. Here, we show that Streptomyces spores are capable of utilizing the motility machinery of other soil bacteria and are transported on the centimeter scale. Motility assays and microscopy studies reveal that Streptomyces spores are transported to plant tissues by interacting directly with the flagella of both gram-positive and gram-negative bacteria. Genetics experiments demonstrate that this form of motility, called piggy-backing, is facilitated by conserved structural proteins present on the surface of Streptomyces spores. These results demonstrate that non-motile bacteria are capable of utilizing the motility machinery of other microbes to complete necessary stages of their lifecycle, and that this mode of transport may be ubiquitous in nature.

microbiology↗