Stress-induced formation of cell wall-deficient cells in filamentous actinomycetes

Ramijan, Karina; Ultee, Eveline; Willemse, Joost; Zhang, Zheren; Wondergem, Joeri A. J.; Meij, Anne van der; Heinrich, Doris; Briegel, Ariane; Wezel, Gilles P. van; Claessen, Dennis

doi:10.1038/s41467-018-07560-9

Cited by 54 publications

(66 citation statements)

References 48 publications

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“…Consistent with fluoxetine-associated increases in expression of sporulation-related genes, imaging of T. sanguinis exposed to 5-HT with fluoxetine revealed punctate staining of the membrane dye FM 4-64 ( Fig. 3f, g), a phenotype observed during spore formation 18 . Notably, fluoxetine treatment in the absence of 5-HT yielded little change in T. sanguinis gene expression (Supplementary Tables 6 and 7), indicating that 5-HT is required for fluoxetine-induced alterations in gene expression.…”

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confidence: 59%

Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut

et al. 2019

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The gut microbiota regulates levels of serotonin (5-hydroxytryptamine, 5-HT) in the intestinal epithelium and lumen 1-5. However, whether 5-HT plays a functional role in bacteria from the gut microbiota remains unknown. We demonstrate that elevating levels of intestinal lumenal 5-HT by oral supplementation or by genetic deficiency in the host 5-HT transporter (SERT) increases the relative abundance of spore-forming members of the gut microbiota, which were previously reported to promote host 5-HT biosynthesis. Within this microbial community, we identify Turicibacter sanguinis as a gut bacterium that expresses a neurotransmitter sodium symporter (NSS)-related protein with sequence and structural homology to mammalian SERT. T. sanguinis imports 5-HT through a mechanism that is inhibited by the selective 5-HT reuptake inhibitor, fluoxetine. 5-HT reduces expression of sporulation factors and membrane transporters in T. sanguinis, which is reversed by fluoxetine exposure. Treating T. sanguinis with 5-HT or fluoxetine modulates its competitive colonization in the gastrointestinal tract of antibiotic-treated mice. In addition, fluoxetine reduces the membership of T. sanguinis in the gut microbiota of conventionally-colonized mice. Host association with T. sanguinis alters intestinal expression of multiple gene pathways, including those important for lipid and steroid metabolism, with corresponding reductions in host systemic triglyceride levels and inguinal adipocyte size. Altogether, these findings support the notion that select bacteria indigenous to the gut microbiota signal bidirectionally with the host serotonergic system to promote their fitness in the intestine. Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

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confidence: 59%

Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut

et al. 2019

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“…For instance, the compositions of the cell wall are different between members of these genera, and several regulatory proteins required for morphogenesis in Streptomyces are absent in Kitasatospora ( 31 ). We recently described that Kitasatospora viridifaciens releases cell wall-deficient cells, called S-cells, under conditions of hyperosmotic stress ( 32 ). These S-cells are only transiently wall deficient and can switch to the mycelial mode of growth.…”

Section: Introductionmentioning

confidence: 99%

“…These S-cells are only transiently wall deficient and can switch to the mycelial mode of growth. In some cases, however, prolonged exposure to high levels of osmolytes can lead to the emergence of mutants that are able to proliferate in the wall-deficient state as so-called L-forms ( 32 , 33 ). Like S-cells, these L-forms retain the ability to construct functional peptidoglycan based on the observation that removal of the osmolytes from the medium leads to the formation of mycelial colonies.…”

Section: Introductionmentioning

confidence: 99%

“…Even though the procedures used to generate L-forms can markedly differ, their mode of proliferation is conserved across species and largely based on biophysical principles. An imbalance in the cell surface area/volume ratio in cells that increase in size causes strong deformations of the cell membrane, followed by the release of progeny cells by blebbing, tubulation, and vesiculation ( 32 , 38 ). Given that lipid vesicles without any content can proliferate in a manner similar to that observed for L-forms led to the hypothesis that this mode of proliferation may be comparable to that used by early life forms that existed before the cell wall had evolved ( 39 , 40 ).…”

Section: Introductionmentioning

confidence: 99%

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An Alternative and Conserved Cell Wall Enzyme That Can Substitute for the Lipid II Synthase MurG

Zhang

Ramijan

Carrión

et al. 2021

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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 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 homologue, which encodes a putative enzyme that shares only around 31% amino acid sequence identity with MurG. We show that this enzyme can replace the canonical MurG, and we therefore designated it MglA. Orthologues of mglA are present in 38% of all genomes of Kitasatospora and members of the sister genus Streptomyces. CRISPR interference experiments showed that K. viridifaciens mglA can also functionally replace murG in Streptomyces coelicolor, thus validating its bioactivity and demonstrating that it is active in multiple genera. All together, these results identify MglA as a bona fide lipid II synthase, thus demonstrating plasticity in cell wall synthesis. IMPORTANCE Almost all bacteria are surrounded by a cell wall, which protects cells from environmental harm. Formation of the cell wall requires the precursor molecule lipid II, which in bacteria is universally synthesized by the conserved and essential lipid II synthase MurG. We here exploit the unique ability of an actinobacterial strain capable of growing with or without its cell wall to discover an alternative lipid II synthase, MglA. Although this enzyme bears only weak sequence similarity to MurG, it can functionally replace MurG and can even do so in organisms that naturally have only a canonical MurG. The observation that MglA proteins are found in many actinobacteria highlights the plasticity in cell wall synthesis in these bacteria and demonstrates that important new cell wall biosynthetic enzymes remain to be discovered.

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“…While historically categorized as free-living saprophytes, recent work on the root microbiome suggests that many Actinobacteria may have a less well understood phase of development or lifestyle associated with the endosphere, which leads to alternate functions and potentially even changes in cellular morphology (Ramijan et al, 2018;van der Meij et al, 2018). It is known that some bacteria occupy different niches (i.e., play different functional roles) depending on the presence of certain environmental triggers, such as carbon sources (Duffy and Défago, 1999;Sánchez et al, 2010).…”

Section: Actinobacterial Enrichment Under Drought Is Not Driven By Romentioning

confidence: 99%

Drought Drives Spatial Variation in the Millet Root Microbiome

et al. 2020

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Efforts to boost crop yield and meet global food demands while striving to reach sustainability goals are hindered by the increasingly severe impacts of abiotic stress, such as drought. One strategy for alleviating drought stress in crops is to utilize rootassociated bacteria, yet knowledge concerning the relationship between plant hosts and their microbiomes during drought remain under-studied. One broad pattern that has recently been reported in a variety of monocot and dicot species from both native and agricultural environments, is the enrichment of Actinobacteria within the drought-stressed root microbiome. In order to better understand the causes of this phenomenon, we performed a series of experiments in millet plants to explore the roles of drought severity, drought localization, and root development in provoking Actinobacteria enrichment within the root endosphere. Through 16S rRNA ampliconbased sequencing, we demonstrate that the degree of drought is correlated with levels of Actinobacterial enrichment in four species of millet. Additionally, we demonstrate that the observed drought-induced enrichment of Actinobacteria occurs along the length of the root, but the response is localized to portions of the root experiencing drought. Finally, we demonstrate that Actinobacteria are depleted in the dead root tissue of Japanese millet, suggesting saprophytic activity is not the main cause of observed shifts in drought-treated root microbiome structure. Collectively, these results help narrow the list of potential causes of drought-induced Actinobacterial enrichment in plant roots by showing that enrichment is dependent upon localized drought responses but not root developmental stage or root death.

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Stress-induced formation of cell wall-deficient cells in filamentous actinomycetes

Cited by 54 publications

References 48 publications

Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut

Intestinal serotonin and fluoxetine exposure modulate bacterial colonization in the gut

An Alternative and Conserved Cell Wall Enzyme That Can Substitute for the Lipid II Synthase MurG

Drought Drives Spatial Variation in the Millet Root Microbiome

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