Biosynthesis and function of cell-surface polysaccharides in the social bacterium Myxococcus xanthus

Pérez‐Burgos, María; Søgaard‐Andersen, Lotte

doi:10.1515/hsz-2020-0217

Cited by 21 publications

(24 citation statements)

References 106 publications

(214 reference statements)

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“…Agents align with one another on collisions (15) and follow paths left by other agents. These biologically relevant paths are called slime trails composed of poorly characterized material consisting of polysaccharides and lipids that are deposited by gliding M. xanthus cells (29)(30)(31)(32)(33). Previously, this model was shown to result in CA formation when the slime-trail following was strong and cells did not reverse (15).…”

Section: The Biophysical Model Reveals Cas Only Arise From Non-reversing Agentsmentioning

confidence: 99%

Emergent myxobacterial behaviors arise from reversal suppression induced by kin contacts

Balagam

Cao

et al. 2021

Preprint

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A wide range of biological systems - from microbial swarms to bird flocks, display emergent behaviors driven by coordinated movement of individuals. To this end, individual organisms interact by recognizing their kin and adjusting their motility based on others around them. However, even in the best-studied systems, the mechanistic basis of the interplay between kin recognition and motility coordination is not understood. Here, using a combination of experiments and mathematical modeling, we uncover the mechanism of an emergent social behavior in Myxococcus xanthus. By overexpressing the cell surface kin recognition receptors, TraA and TraB, large numbers of cells adhere to one another and form organized macroscopic circular aggregates that spin clockwise or counterclockwise. Mechanistically, TraAB adhesion results in sustained cell-cell contacts that signal the Frz chemosensory pathway. In turn, cell reversals are suppressed and circular aggregates form as the result of cells' ability to follow cellular slime trails. Furthermore, our in-silico simulations demonstrate a remarkable ability to predict self-organization patterns when phenotypically distinct strains are mixed. Therefore, this work provides key mechanistic insights into M. xanthus social interactions and demonstrates how social recognition transforms physical interactions into emergent collective behaviors.

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Section: The Biophysical Model Reveals Cas Only Arise From Non-reversing Agentsmentioning

confidence: 99%

Emergent myxobacterial behaviors arise from reversal suppression induced by kin contacts

Balagam

Cao

et al. 2021

Preprint

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“…Certain HMW polysaccharides do not remain associated with the cell surface and are instead secreted to the extracellular milieu where they can influence bacterial physiology (Saïdi et al ., 2021, Islam et al ., 2020). In both monoderm (Gram-positive) and diderm (Gram-negative) bacteria, multiple secreted polymers often act in concert to modulate complex physiology (Pérez-Burgos & Søgaard-Andersen, 2020, Lavelle et al ., 2021, Franklin et al ., 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Under nutrient deprivation, cells in a swarm biofilm form myxospore- filled fruiting bodies through a developmental program resulting in a differentiated cell community (Muñoz-Dorado et al ., 2016). This complex lifecycle is modulated by the secretion of three known polysaccharides (Pérez-Burgos & Søgaard-Andersen, 2020). Cells constitutively produce EPS, a specific surface-associated polymer that forms a glycocalyx surrounding the cell body (Saïdi et al ., 2021) and which constitutes the main matrix component in biofilms of this bacterium (Hu et al ., 2013, Smaldone et al ., 2014).…”

Section: Introductionmentioning

confidence: 99%

Bacterial outer-membrane polysaccharide export (OPX) proteins occupy three structural classes with selective β-barrel porin requirements for polymer secretion

Saïdi

Mahanta

Panda

et al. 2022

Preprint

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Secretion of high-molecular-weight polysaccharides across the bacterial envelope is ubiquitous as it enhances prokaryotic survival in (a)biotic settings. Such polymers are often assembled by Wzx/Wzy- or ABC transporter-dependent schemes that implicate outer-membrane (OM) polysaccharide export (OPX) proteins in polymer translocation to the cell surface. In the social predatory bacterium Myxococcus xanthus, exopolysaccharide (EPS)-pathway WzaX, major spore coat (MASC)-pathway WzaS, and biosurfactant polysaccharide-pathway WzaB were herein found to be truncated OPX homologues of Escherichia coli Wza lacking OM-spanning α-helices. Comparative genomics across all bacteria, complemented with cryo-electron tomography cell-envelope analyses, revealed WzaX/S/B architecture to be the most common amongst three defined OPX-protein structural classes independent of periplasmic thickness. Fold-recognition and deep-learning analyses revealed the conserved M. xanthus proteins MXAN_7418/3226/1916 (encoded adjacent to WzaX/S/B) to be integral OM β-barrels, with structural homology to the poly-N-acetyl-D-glucosamine synthase-dependent pathway porin PgaA. Such porins were identified in bacteria near numerous genes for all three OPX-protein classes. Interior MXAN_7418/3226/1916 β-barrel electrostatics were found to match known properties of their associated polymers. With MXAN_3226 essential for MASC export, and MXAN_7418 absence shown herein to compromise EPS translocation, these data support a novel secretion paradigm for Wzx/Wzy-dependent pathways in which those containing an OPX component that cannot span the OM instead utilize a β-barrel porin to mediate polysaccharide transport across the OM.

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“…EPS secretion is an important strategy for environmental adaption of bacteria (78). With enormous varieties of chemical compositions, molecular weight, and adherence to bacterial surfaces, these molecules serve a wide variety of purposes, including as important components of the bacterial cell envelope (4, 26, 32), providing protection against desiccation and toxic substances (78–80), mediating attachment to surfaces (78, 81), biofilm formation (82–83), host interaction (84–85), and bacterial motility (53, 56). Although there are many methods for detection of bacterial EPS, relatively little is known about the chemical composition, synthesis, and secretion of these molecules.…”

Section: Discussionmentioning

confidence: 99%

“…Despite these differences, secretion of both protein and EPS pose similar challenges to the cell, as bulky, hydrophilic, high-molecular-weight polymers are translocated across hydrophobic membranes. So far, three different mechanisms have been described for EPS secretion in Gram-negative bacteria ( 28, for a review in Myxococcus xanthus see 32 ): the Wzx/Wzy, the ABC transporter, and the synthase-dependent secretion pathways. The Wzx/Wzy pathway is used by bacteria for the synthesis of group I capsular exopolysaccharide, O-antigen lipopolysaccharide (LPS) and succinoglycan EPS, which are synthesized from sugar phosphates that bind to a carrier lipid in the cytoplasmic membrane (26–28).…”

Section: Introductionmentioning

confidence: 99%

Type two secretion systems secretins are necessary for exopolymeric slime secretion in cyanobacteria and myxobacteria

Zuckerman

Hoiczyk

2022

Preprint

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While protein translocation in Gram-negative bacteria is well understood, our knowledge about the translocation of other high-molecular-weight substances is limited. Nozzle-like structures that secrete exopolymeric substances during gliding motility have previously been observed in the outer membranes of cyanobacteria and myxobacteria. Here, we show that these nozzles are composed of the secretins PilQ/GspD, the outer membrane component of the type II and III secretion systems, the type IV pilus apparatus, and filamentous phage extrusion machinery. Our results show for the first time that secretins may be used for secretion of non-proteinaceous polymers in some bacteria, considerably expanding the repertoire of substrates of these multifunctional outer membrane gates. Moreover, we show that gspD is an essential gene in Myxococcus xanthus, which, when depleted, renders this bacterium defective in slime secretion and gliding motility.SignificanceMany bacteria exhibit gliding motility, movement across surfaces. This motility has been correlated with the deposit of slime trails in their wake. To date, the mechanism of slime secretion has not been understood, and no cell envelope-structures have been identified that are involved in slime secretion during gliding motility. Here, we show that cyanobacteria and myxobacteria use the secretins PilQ/GspD, the outer membrane channels of the T2SS, for slime secretion, which demonstrates a novel cargo transport capacity of these multifunctional outer membrane gates.

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Biosynthesis and function of cell-surface polysaccharides in the social bacterium Myxococcus xanthus

Cited by 21 publications

References 106 publications

Emergent myxobacterial behaviors arise from reversal suppression induced by kin contacts

Emergent myxobacterial behaviors arise from reversal suppression induced by kin contacts

Bacterial outer-membrane polysaccharide export (OPX) proteins occupy three structural classes with selective β-barrel porin requirements for polymer secretion

Type two secretion systems secretins are necessary for exopolymeric slime secretion in cyanobacteria and myxobacteria

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