image: Pv1-induced learned avoidance causes avoidance of P. mendocina, a beneficial natural bacterial species. Schematic outlining the findings of the study. Prior to exposure to pathogenic P. vranovensis, worms are naively attracted to both P. vranovensis, and the non-pathogenic P. mendocina. Exposure to P. vranovensis or to the Pv1 small RNA of P. vranovensis induces learned avoidance of P. vranovensis in worms and four generations of progeny. Exposed worms not only avoid the pathogenic P. vranovensis, but also the non-pathogenic P. mendocina. Schematic was created using Biorender. Each dot represents an individual choice assay plate (B-F). Boxplots: center line, median; box range, 25th–75th percentiles; whiskers denote minimum-maximum values. One-way ANOVA with Tukey’s multiple comparison’s test, **p<0.01, ns, not significant (B); Unpaired, two-tailed Student’s t test, **p<0.01, ***p<0.001 (D-F). For the survival assay in (A), ***p<0.001 (by Log-rank (Mantel-Cox) test for survival).
Credit: Murphy et al., 2024, PLOS Genetics, CC-BY 4.0 (https://creativecommons.org/licenses/by/4.0/)
The nematode worm C. elegans will stay away from dangerous bacteria in its environment when exposed to certain bacterial RNAs—and can transmit that learned behavior to future generations. A team led by Coleen Murphy at Princeton University report these findings in a new study, published March 28 in the journal PLOS Genetics.
Previous experiments have shown that C. elegans can learn and remember a strain of the bacterium Pseudomonas aeruginosa that causes infections in humans. Even though that avoidance behavior is not encoded in the genes, worms can pass on that information to its progeny for four generations through a phenomenon called transgenerational inheritance. While this phenomenon has been demonstrated under lab conditions, it was unknown whether wild worms would have a similar reaction to harmful bacteria that they encounter in their natural environment.
Murphy’s team screened bacteria that live alongside C. elegans in the wild, and found that another Pseudomonas bacteria, called Pseudomonas vranovensis, also causes the worms to avoid it after exposure. Furthermore, they identified a small RNA produced by the bacteria that activates this behavior by altering gene expression in the worm’s nervous system. The researchers hypothesize that the reason the behavior ceases after a few generations is because the response also causes the worms to avoid a helpful bacterium, Pseudomonas mendocina, which is a good food source.
The new findings provide proof of principle that the transgenerational inheritance previously observed in the lab likely benefits nematodes in the wild as well. The study also adds to our understanding of how small molecules from bacteria can regulate interactions between the bacteria and their worm hosts. The researchers propose that identifying bacterial small molecules with similar effects will allow us to further explore this new type of bacteria-host interaction and its role in worm survival.
The authors add: “Here, Sengupta and colleagues report that a pathogenic bacterial species found in C. elegans' natural environment, Pseudomonas vranovensis, induces learned avoidance behavior and four generations of transgenerational inheritance of avoidance in worms through a single small RNA. Worms exposed to this small RNA (Pv1) not only avoid the pathogen, but also other beneficial bacteria (Pseudomonas mendocina), suggesting ecological trade-offs for such heritable behaviors in the wild that may lead to the cessation of avoidance after several generations.”
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In your coverage, please use this URL to provide access to the freely available article in PLOS Genetics:
http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1011178
Citation: Sengupta T, St. Ange J, Kaletsky R, Moore RS, Seto RJ, Marogi J, et al. (2024) A natural bacterial pathogen of C. elegans uses a small RNA to induce transgenerational inheritance of learned avoidance. PLoS Genet 20(3): e1011178. https://doi.org/10.1371/journal.pgen.1011178
Author Countries: United States
Funding: This work was supported by a Pioneer Award to CTM (NIGMS DP1GM119167), a Transformative R01 Award (1R01AT011963-01) to ZG & CTM., CDCP 75D30122C15113 to CM, T32GM007388 (NIGMS) support of RSM., a Damon Runyon Fellowship (DRG-2481-22) to TS, a Ford Foundation Predoctoral Fellowship to RS (https://www.nationalacademies.org/our-work/ford-foundation-fellowships), and an NSF GRFP (DGE-2039656) predoctoral award to JS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Journal
PLOS Genetics
Method of Research
Experimental study
Subject of Research
Animals
COI Statement
Competing Interests: I have read the journal’s policy and the authors of this manuscript have the following competing interests: ZG is the founder of ArrePath.