Bacterial Swarmers Enriched During Intestinal Stress Ameliorate Damage

De, Arpan; Chen, Weijie; Li, Hao; Wright, Justin; Lamendella, Regina; Lukin, Dana J.; Szymczak, Wendy; Sun, Katherine; Kelly, Libusha; Ghosh, Subho; Kearns, Daniel B.; He, Zhen; Jobin, Christian; Li, Xiaoping; Byju, Arjun; Chatterjee, Shirshendu; Yeoh, Beng San; Vijay‐Kumar, Matam; Tang, Jay X.; Prajapati, Milankumar; Bartnikas, Thomas B.; Mani, Sridhar

doi:10.1053/j.gastro.2021.03.017

Cited by 25 publications

(38 citation statements)

References 47 publications

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“…First, we rule out cell density difference as the reason for the difference in the confined motion patterns by concentrating planktonic cells to a comparable density of a naturally expanding swarm on agar (see Methods) before mounting the PDMS chip. Second, we noticed that SM3 tends to get elongated when they swarm (De et al, 2021). We hypothesize that elongated bacteria may enhance the local alignment of the rod-shaped cells and increase the vortex size in mesoscale turbulence (Doostmohammadi, Adamer, Thampi, & Yeomans, 2016;Peruani, Deutsch, & Bar, 2006).…”

Section: The Large Single Swirl Behavior Is Indicative Of Cell-cell Interactionmentioning

confidence: 78%

“…The beads' motion is not a perfect swirl in every well on the colitic tissue because the mucosal surface is not as smooth as the agar surface. There are sags and crests on the inflamed mucosal surface due to the disrupted mucin layer (De et al, 2021). We conjectured that this unevenness hindered the swirl formation to a certain extent.…”

Section: Discussionmentioning

confidence: 93%

“…Compared with previous work, our experimental setup has the advantage of ensuring stable and sustainable patterns. First, PDMS material does not harm living bacteria cells and is permeable to oxygen (Turner, Zhang, Darnton, & Berg, 2010), thus ensuring continued oxygen exposure required for swarming (De et al, 2021). Second, we mounted the microchip on a soft agar containing over 97% water by mass, which automatically fills the wells via permeability and capillary flow.…”

Section: Discussionmentioning

confidence: 99%

“…A novel bacterial strain Enterobacter sp. SM3 (NCBI BioProject PRJNA558971), isolated in 2014 from mice with colitis induced with dextran sulfate sodium (DSS), has been previously studied for motility (Araujo, Chen, Mani, & Tang, 2019) and host phenotype (De et al, 2021). SM3 expands rapidly on 0.5% agar with the collective motion of multilayers of cells at the edge.…”

Section: Swarming Enterobacter Sp Sm3 Forms Large Single Swirlsmentioning

confidence: 99%

“…For instance, studies show that compared with swimming cells, the requirement for flagella torque is higher for swarming B. subtilis (Hall, Subramanian, Oshiro, Canzoneri, & Kearns, 2018); swarming E. coli remodel their chemotaxis pathway (Partridge, Nhu, Dufour, & Harshey, 2019); and in swarming P. aeruginosa, both the production of virulence factors and antibiotic resistance increase (Overhage, Bains, Brazas, & Hancock, 2008). A recent study has demonstrated a medically relevant distinction between swarming and swimming: a particular strain of swarming Enterobacter protects against mice intestinal inflammation while its swarm-deficient counterpart does not (De et al, 2021). The evidence to date that shows swarming to be different from swimming comes mostly from biological data (Kearns, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Confinement discerns swarmers from planktonic bacteria

Chen

Mani

Karani

et al. 2021

eLife

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Powered by flagella, many bacterial species exhibit collective motion on a solid surface commonly known as swarming. As a natural example of active matter, swarming is also an essential biological phenotype associated with virulence, chemotaxis, and host pathogenesis. Physical changes like cell elongation and hyper flagellation have been shown to accompany the swarming phenotype. Less studied, however, are the contrasts of collective motion between the swarming cells and their counterpart planktonic cells of comparable cell density. Here, we show that confining bacterial movement in circular microwells allows distinguishing bacterial swarming from collective swimming. On a soft agar plate, a novel bacterial strain Enterobacter sp. SM3 in swarming and planktonic states exhibited different motion patterns when confined to circular microwells of a specific range of sizes. When the confinement diameter was between 40 μm and 90 μm, swarming SM3 formed a single swirl motion pattern in the microwells whereas planktonic SM3 formed multiple swirls. Similar differential behavior is observed across several other species of gram-negative bacteria. We also observed 'rafting behavior' of swarming bacteria upon dilution. We hypothesize that the rafting behavior might account for the motion pattern difference. We were able to predict these experimental features via numerical simulations where swarming cells are modeled with stronger cell-cell alignment interaction. Our experimental design using PDMS microchip disk arrays enabled us to observe bacterial swarming on murine intestinal surface suggesting a new method for characterizing bacterial swarming under complex environments, such as in polymicrobial niches, and for in vivo swarming exploration.

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Section: The Large Single Swirl Behavior Is Indicative Of Cell-cell Interactionmentioning

confidence: 78%

Section: Discussionmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Swarming Enterobacter Sp Sm3 Forms Large Single Swirlsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Confinement discerns swarmers from planktonic bacteria

Chen

Mani

Karani

et al. 2021

eLife

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Oral Delivery of Bioactive Glass‐Loaded Core–Shell Hydrogel Microspheres for Effective Treatment of Inflammatory Bowel Disease

et al. 2023

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Resolving inflammation and promoting intestinal tissue regeneration are critical for inflammatory bowel disease (IBD) treatment. Bioactive glass (BG) is a clinically approved bone graft material and has been shown to modulate inflammatory response, but it is unknown whether BG can be applied to treat IBD. Here, it is reported that BG attenuates pro-inflammatory response of lipopolysaccharide (LPS)-stimulated macrophages and hence reduces inflammatory damage to intestinal organoids in vitro. In addition, zein/sodium alginate-based core-shell microspheres (Zein/SA/BG) are developed for oral delivery of BG, which helps prevent premature dissolution of BG in the stomach. The results show that Zein/SA/BG protects BG from a gastric-simulated environment while dissolved in an intestinal-simulated environment. When administered to acute and chronic colitis mice model, Zein/SA/BG significantly reduces intestinal inflammation, promotes epithelial tissue regeneration, and partially restores microbiota homeostasis. These findings are the first to reveal the therapeutic efficacy of BG against IBD, which may provide a new therapeutic approach at low cost for effective IBD treatment.

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Gut microbiome and bladder cancer: A new link through nitrosamine metabolism

Mani

2024

Cell Host & Microbe

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Bacterial Swarmers Enriched During Intestinal Stress Ameliorate Damage

Cited by 25 publications

References 47 publications

Confinement discerns swarmers from planktonic bacteria

Confinement discerns swarmers from planktonic bacteria

Oral Delivery of Bioactive Glass‐Loaded Core–Shell Hydrogel Microspheres for Effective Treatment of Inflammatory Bowel Disease

Gut microbiome and bladder cancer: A new link through nitrosamine metabolism

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