Synergistic interaction of gut microbiota enhances the growth of nematode through neuroendocrine signaling

Lo, Wen‐Sui; Han, Ziduan; Witte, Hanh; Röseler, Waltraud; Sommer, Ralf J.

doi:10.1016/j.cub.2022.03.056

Cited by 11 publications

(20 citation statements)

References 69 publications

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“…Furthermore, in C. elegans , developmental dependent expression of Cel-daf-7 is observed with expression evident in the amphid neurons of the L1 and L2 larvae preceding the dauer stage but not in the dauer larvae itself ( Ren et al 1996 ). We therefore utilized previously generated Ppa-daf-7.1 and Ppa-daf-7.2 transcriptional reporters ( Lo et al 2022 ) to investigate any similar developmental restricted expression patterns in P. pacificus . However, both reporters showed robust and consistent expression in amphid neurons in both well-fed J2 and starvation-induced dauer larvae in P. pacificus indicating distinct regulation of daf-7 between species ( supplementary fig.…”

Section: Resultsmentioning

confidence: 99%

“…In Ppa-daf-7.1; Ppa-daf-7.2 double mutants, the Eu mouth-form ratio decreased from over 97% in wild-type animals to 66% in the mutant strain. As Ppa-daf-7.1 and Ppa-daf-7.2 are expressed in head sensory neurons ( Lo et al 2022 ) and have previously also been shown to be defective in their response to MM ( fig. 2 E ), we hypothesize that the altered mouth-form ratio may also be caused by an inability to sense environmental cues.…”

Section: Resultsmentioning

confidence: 99%

“…As such, several TGF-β family members have been identified in parasitic nematodes, although functional studies are problematic due to the complex life cycles found in these organisms ( McSorley et al 2009 ; Ogawa et al 2009 ; Crook et al 2010 ; Ma et al 2019 ; Yang et al 2019 ; He et al 2020 ). Interestingly, a recent study in P. pacificus demonstrated that the Ppa-daf-7 pathway is necessary for bacterial induced gut–brain communication, which in turn enhanced numerous developmental phenotypes ( Lo et al 2022 ). Moreover, multiple daf-7 -type signaling ligands have been identified suggesting a previously unknown element to TGF-β signaling including the possibility of its neofunctionalization outside of the canonical C. elegans pathway.…”

Section: Introductionmentioning

confidence: 99%

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Evolution and Diversity of TGF-β Pathways are Linked with Novel Developmental and Behavioral Traits

Roca²,

Dardiry

et al. 2022

Molecular Biology and Evolution

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Transforming growth factor β (TGF-β) signalling is essential for numerous biological functions. It is a highly conserved pathway found in all metazoans including the nematode Caenorhabditis elegans, which has also been pivotal in identifying many components. Utilising a comparative evolutionary approach, we explored TGF-β signalling in nine nematode species and revealed striking variability in TGF-β gene frequency across the lineage. Of the species analysed, gene duplications in the DAF-7 pathway appear common with the greatest disparity observed in Pristionchus pacificus. Specifically, multiple paralogues of daf-3, daf-4 and daf-7 were detected. To investigate this additional diversity, we induced mutations in 22 TGF-β components and generated corresponding double, triple and quadruple mutants revealing both conservation and diversification in function. Although, the DBL-1 pathway regulating body morphology appears highly conserved, the DAF-7 pathway exhibits functional divergence, notably in some aspects of dauer formation. Furthermore, the formation of the phenotypically plastic mouth in P. pacificus is partially influenced through TGF-β with the strongest effect in Ppa-tag-68. This appears important for numerous processes in P. pacificus but has no known function in C. elegans. Finally, we observe behavioural differences in TGF-β mutants including in chemosensation and the establishment of the P. pacificus kin-recognition signal. Thus, TGF-β signalling in nematodes represents a stochastic genetic network capable of generating novel functions through the duplication and deletion of associated genes.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Evolution and Diversity of TGF-β Pathways are Linked with Novel Developmental and Behavioral Traits

Roca²,

Dardiry

et al. 2022

Molecular Biology and Evolution

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“…However, microbiota represent a complex network of bacterial communities with sophisticated dynamics and successions, representing a major challenge for disentangling functional interactions in ecosystems. Bacterial-feeding nematodes are favourable organisms to study hostmicrobiota interactions due to their simple anatomy, rapid generation time and powerful molecular tools (Dirksen et al 2016;Lo, Han, et al 2022;Zhang et al 2017). In the model nematode Caenorhabditis elegans, multiple studies have demonstrated that single bacterial strains can greatly alter host physiology (Samuel et al 2016).…”

Section: Introductionmentioning

confidence: 99%

“…The free-living microbial-feeding and predatory nematode Pristionchus pacificus has been developed as a model along with C. elegans to study various organismal traits, including developmental traits, predation, nutrition and immunity (Lightfoot et al 2019a;Ragsdale et al 2013a;Lo, Han, et al 2022;Akduman et al 2020). Although P. pacificus and C. elegans are both soil nematodes that can feed on microbes derived from decomposing organic matter, they have distinct ecological niches.…”

Section: Introductionmentioning

confidence: 99%

Microbiota Succession Influences Nematode Physiology in a Beetle Microcosm Ecosystem

Han

Sommer

2023

Preprint

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Research during the last decade has generated a substantial understanding of the role of microbiota in animal development, metabolism and immunity, including humans. However, many organismal interactions involve microbial successions, such as in animal decay but also human health and disease. The complexity of most microbiota makes it difficult to obtain insight into such microbial successions, resulting in a limited understanding of microbiota for ecosystem functioning. One potential, relatively simple, model system for the analysis of microbial successions is insect decay in soil ecosystems, a highly abundant process that has however, not been investigated in detail. For example, microbiota and nematodes are the two most abundant groups of organisms in soil systems, but their interplay and successions during the decomposition of insects are currently unknown. Here, we use a semi-artificial decaying rose chafer grub microcosm to study the reciprocal interactions between microbiota and nematodes through metagenomics and transcriptomic studies. We show that the controlled addition of nematodes to beetle grub carcasses will strongly influence the microbial succession and result in a massive increase in microbial diversity. Nematodes select microbes of high nutritional value for consumption, thereby influencing the composition of microbiota on the decaying insect. Reciprocally, the activity of nematode metabolic pathways strongly responds to their microbial diet and affects fat metabolism and the formation of dauer larvae, the nematode dispersal stage. These results indicate the importance of microbial successions and their reciprocal interactions with nematodes for insect decay in soil ecosystems.

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Microbiomes: How a gut bacterium promotes healthier living in a nematode

MacNeil

2022

Current Biology

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Synergistic interaction of gut microbiota enhances the growth of nematode through neuroendocrine signaling

Cited by 11 publications

References 69 publications

Evolution and Diversity of TGF-β Pathways are Linked with Novel Developmental and Behavioral Traits

Evolution and Diversity of TGF-β Pathways are Linked with Novel Developmental and Behavioral Traits

Microbiota Succession Influences Nematode Physiology in a Beetle Microcosm Ecosystem

Microbiomes: How a gut bacterium promotes healthier living in a nematode

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