The Assembly of Bacteria Living in Natural Environments Shapes Neuronal Integrity and Behavioral Outputs in Caenorhabditis elegans

Urquiza-Zurich, Sebastian; García-Angulo, Víctor Antonio; Burdisso, Paula; Palominos, M. Fernanda; Fernandez-Hubeid, Lucia E.; Harcha, Paloma A.; Castillo, Juan P.; Calixto, Andrea

doi:10.1128/mbio.03402-22

Cited by 4 publications

(4 citation statements)

References 50 publications

(62 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Food availability and microbiota composition affect neuronal integrity and survival ( Caneo et al, 2019 ; Liu et al, 2020 ; Urrutia et al, 2020 ; Shandilya et al, 2022 ; Zhang et al, 2022 ; Urquiza-Zurich et al, 2023 ). To find commonalities between these two neuroprotective conditions, we study gene expression, calcium contribution, and mitochondrial parameters in the AVM neuron of C. elegans .…”

Section: Discussionmentioning

confidence: 99%

Microbiota and Diapause-Induced Neuroprotection Share a Dependency on Calcium But Differ in Their Effects on Mitochondrial Morphology

Delgado

Urrutia

Gutzwiller

et al. 2023

eNeuro

Self Cite

View full text Add to dashboard Cite

The balance between the degeneration and regeneration of damaged neurons depends on intrinsic and environmental variables. In nematodes, neuronal degeneration can be reversed by intestinal GABA and lactate-producing bacteria, or by hibernation driven by food deprivation. However, it is not known whether these neuroprotective interventions share common pathways to drive regenerative outcomes. Using a well-established neuronal degeneration model in the touch circuit of the bacterivore nematodeCaenorhabditis elegans,we investigate the mechanistic commonalities between neuroprotection offered by the gut microbiota and hunger-induced diapause. Using transcriptomics approaches coupled to reverse genetics, we identify genes that are necessary for neuroprotection conferred by the microbiota. Some of these genes establish links between the microbiota and calcium homeostasis, diapause entry, and neuronal function and development. We find that extracellular calcium as well as mitochondrial MCU-1 and reticular SCA-1 calcium transporters are needed for neuroprotection by bacteria and by diapause entry. While the benefits exerted by neuroprotective bacteria requires mitochondrial function, the diet itself does not affect mitochondrial size. In contrast, diapause increases both the number and length of mitochondria. These results suggest that metabolically-induced neuronal protection may occur via multiple mechanisms.Significance statementCalcium signaling and mitochondrial function have recently been suggested to promote axonal growth following neuronal damage, but the underlying mechanisms and physiological significance are unclear. Combining transcriptomics, genetics and cell biological approaches in a simple animal model of axonal degeneration and regeneration, we demonstrate that neuronal repair conferred by two different metabolic processes occurs in diverse ways, requiring differential changes in mitochondrial function and calcium homeostasis. Furthermore, this work shows that neuroprotection can be additive, providing a new conceptual framework for developing therapeutic interventions in neurodegenerative conditions that leverage the intersection of metabolism, microbiota and mitochondrial function.

show abstract

Section: Discussionmentioning

confidence: 99%

Microbiota and Diapause-Induced Neuroprotection Share a Dependency on Calcium But Differ in Their Effects on Mitochondrial Morphology

Delgado

Urrutia

Gutzwiller

et al. 2023

eNeuro

Self Cite

View full text Add to dashboard Cite

show abstract

“…However, as in humans, in C. elegans its commensal microbial communities play a crucial physiological role. 341 Some naturally associated bacteria influence behaviour, stress- and infection resistance, fecundity, metabolism, and life span of C. elegans ; 342–347 e.g. , different bacterial food sources can cause different uptake/accumulation of flavonoids.…”

Section: Multicomponent Mixtures From Natural Sources With Anti-aging...mentioning

confidence: 99%

The role of Caenorhabditis elegans in the discovery of natural products for healthy aging

et al. 2023

View full text Add to dashboard Cite

show abstract

“…This collaborative effort prompted the creation of the C. elegans Microbiome (CeMbio), a model microbiome consisting of the 12 most abundant gut bacteria families naturally associated with C. elegans (Dirksen et al 2020, 202). Individual isolates from this consortium are known to affect growth, food choice behavior, and physiology, as well neural degradation through metabolite secretion (Chen et al 2022; Kohar Annie B. Kissoyan et al 2022; Urquiza-Zurich et al 2023; Carola Petersen et al 2021; Chai et al 2024). However, these studies only consider the influence and composition of CeMbio bacteria in the gut and have not examined their potential impact at other body sites like the cuticle.…”

Section: Introductionmentioning

confidence: 99%

“…Individual isolates from this consortium are known to affect growth, food choice behavior, and physiology, as well neural degradation through metabolite secretion (Chen et al 2022; Kohar Annie B. Kissoyan et al 2022;Urquiza-Zurich et al 2023;Carola Petersen et al 2021;Chai et al 2024). However, these studies only consider the influence and composition of CeMbio bacteria in the gut and have not examined their potential impact at other body sites like the cuticle.…”

Section: Introductionmentioning

confidence: 99%

Identification and characterization of a skin microbiome onCaenorhabditis eleganssuggests environmental microbes confer cuticle protection

Haghani,

Lampe,

Samuel

et al. 2024

Preprint

View full text Add to dashboard Cite

In the wild,C. elegansare emersed in environments teeming with a veritable menagerie of microorganisms. TheC. eleganscuticular surface serves as a barrier and first point of contact with this microbial milieux. Here, we identify microbes fromC. elegansnatural habitats that associate with its cuticle, constituting a simple ‘skin microbiome’. We rear our animals on a modified CeMbio, mCeMbio, a consortium of ecologically relevant microbes. We first combine standard microbiological methods with an adapted micro skin-swabbing tool to describe the skin-resident bacteria on theC. eleganssurface. Further, we conduct 16S rRNA gene sequencing studies to identify relative shifts in the proportion of mCeMbio bacteria upon surface-sterilization, implying distinct skin-and gut-microbiomes. We find that some strains of bacteria, includingEnterobacter sp.JUb101, are primarily found on the nematode skin, while others likeStenotrophomonas indicatrixJUb19 andOchrobactrum vermisMYb71 are predominantly in the animal’s gut. Finally, we show that this skin microbiome promotes host cuticle integrity in harsh environments. Together, we identify a skin microbiome for the well-studied nematode model and propose its value in conferring host fitness advantages in naturalized contexts.ImportanceThe genetic model organismC. eleganshas recently emerged as a tool for understanding host-microbiome interactions. Nearly all of these studies either focus on pathogenic or gut-resident microbes. Little is known about the existence of native, non-pathogenic skin microbes or their function. We show that members of a modifiedC. elegansmodel microbiome, mCeMbio, can adhere to the animal’s cuticle and confer protection from noxious environments. We combine a novel micro-swab tool, the first 16S microbial sequencing data from relatively unperturbedC. elegans, and physiological assays to demonstrate microbially mediated protection of the skin. This work serves as a foundation to explore wildC. elegansskin microbiomes and useC. elegansas a model for skin research.

show abstract

The Assembly of Bacteria Living in Natural Environments Shapes Neuronal Integrity and Behavioral Outputs in Caenorhabditis elegans

Cited by 4 publications

References 50 publications

Microbiota and Diapause-Induced Neuroprotection Share a Dependency on Calcium But Differ in Their Effects on Mitochondrial Morphology

Microbiota and Diapause-Induced Neuroprotection Share a Dependency on Calcium But Differ in Their Effects on Mitochondrial Morphology

The role of Caenorhabditis elegans in the discovery of natural products for healthy aging

Identification and characterization of a skin microbiome onCaenorhabditis eleganssuggests environmental microbes confer cuticle protection

Contact Info

Product

Resources

About