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Interspecies relationships of natural amoebae and bacteria with C. elegans create environments propitious for multigenerational diapause
Indexado
WoS WOS:001448115900001
Scopus SCOPUS_ID:105003568392
DOI 10.1128/MSYSTEMS.01566-24
Año 2025
Tipo artículo de investigación

Citas Totales

Autores Afiliación Chile

Instituciones Chile

% Participación
Internacional

Autores
Afiliación Extranjera

Instituciones
Extranjeras


Abstract



The molecular and physical communication within the microscopic world underpins the entire web of life as we know it. However, how organisms, such as bacteria, amoebae, and nematodes-all ubiquitous-interact to sustain their ecological niches, particularly how their associations generate and influence behavior, remains largely unknown. In this study, we developed a framework to examine long-term interactions between microbes and animals. From soil samples collected in a temperate, semi-arid climate, we isolated culturable bacterial genera, including Comamonas, Stenotrophomonas, Chryseobacterium, and Rhodococcus, as well as the amoeba, Tetramitus. This microbial ensemble was fed to the nematode C. elegans in experiments spanning over 20 nematode generations to assess developmental rate, dauer entry, fertility, and feeding behavior. Our findings reveal that microbes and nematodes create a stable environment where no species are exhausted, and where nematodes enter diapause after several generations. We have termed this phenomenon dauer formation on naturally derived ensembles (DaFNE). DaFNE occurs across a range of optimal temperatures, from 15 degrees C to 25 degrees C, and is dependent on the nematode's pheromone biosynthesis pathway. The phenomenon intensifies with each passing generation, exhibiting both strong intergenerational and transgenerational effects. Moreover, the RNA interference (RNAi) pathway-both systemic and cell-autonomous-is essential for initiating DaFNE, while heritable RNAi effectors are required for its transgenerational effects. These findings indicate that RNA-mediated communication plays a critical role in bacterially induced behaviors in natural environments. IMPORTANCE Microscopic nematodes are the most abundant multicellular animals on Earth, which implies they have evolved highly successful relationships with their associated microbiota. However, little is known about how nematode behavior is influenced within complex ecosystems where multiple organisms interact. In this study, we used four bacteria and an amoeba from a natural ecosystem to explore behavioral responses in the nematode Caenorhabditis elegans over an 8 week period. The most striking finding was the nematodes' commitment to a form of hibernation known as diapause. We have termed this phenomenon dauer formation on naturally derived ensembles (DaFNE). Our results suggest that nematodes in nature may frequently enter hibernation as a result of communication with their microbial partners. DaFNE requires the production of nematode pheromones, as well as the RNA interference pathway, indicating that the RNA communication between nematodes and their microbiota may play a critical role. Interestingly, at higher temperatures, fewer animals are needed to trigger DaFNE, suggesting that a mild increase in temperature may promote diapause in natural environments without causing stress to the animals.

Revista



Revista ISSN
M Systems 2379-5077

Métricas Externas



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Disciplinas de Investigación



WOS
Microbiology
Scopus
Sin Disciplinas
SciELO
Sin Disciplinas

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Publicaciones WoS (Ediciones: ISSHP, ISTP, AHCI, SSCI, SCI), Scopus, SciELO Chile.

Colaboración Institucional



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Autores - Afiliación



Ord. Autor Género Institución - País
1 Serey, Marcela - Universidad de Valparaíso - Chile
2 Retamales, Esteban - Universidad de Valparaíso - Chile
3 Ibanez, Gabriel - Universidad de Valparaíso - Chile
4 Riadi, Gonzalo - Universidad de Talca - Chile
5 Orio, Patricio - Universidad de Valparaíso - Chile
6 CASTILLO, JUAN PABLO Hombre Universidad de Valparaíso - Chile
7 CALIXTO-MOHOR, ANDREA LEONOR Mujer Universidad de Valparaíso - Chile

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Financiamiento



Fuente
FONDECYT
Fondo Nacional de Desarrollo Científico y Tecnológico
National Institutes of Health

Muestra la fuente de financiamiento declarada en la publicación.

Agradecimientos



Agradecimiento
Fondecyt 1220650, 1231357 Andrea Calixto Gonzalo Riadi
We thank Marcela Leg\u00FCe for insightful comments on the manuscript. Rene Z\u00FA\u00F1iga and Carlos Vasconcellos helped with the codes for the time lapse acquisition. Some strains were provided by the CGC, which is funded by NIH Office of Research Infrastructure Programs (P40 OD010440). This work was funded by Fondecyt (Fondo Nactional de Desarollo Cient\u00EDfico y Tecnol\u00F3gico; Grants 1220650 to A.C.; and 1231357 to G.R.) J.P.C. and A.C.: conceptualization; M.S., P.O., G.R., J.P.C., and A.C.: methodology; M.S., E.R., G.I., P.O., G.R., J.P.C., and A.C.: investigation; A.C.: writing: original draft; P.O., J.P.C., and A.C.: writing: review and editing; and A.C.: funding acquisition. Fondecyt 1220650, 1231357 Andrea Calixto Gonzalo Riadi

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