Serotonin Drives Predatory Feeding Behavior via Synchronous Feeding Rhythms in the Nematode <i>Pristionchus pacificus</i>

Okumura, Misako; Wilecki, Martin; Sommer, Ralf J.

doi:10.1534/g3.117.300263

Cited by 30 publications

(56 citation statements)

References 33 publications

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“…Here, P. pacificus exploits the distinct microbial habitat found on the decaying beetle carcass to complete its life cycle [10]. In addition, P. pacificus is an omnivorous nematode capable of feeding on bacteria, fungi, and also predating on other nematodes [11][12][13]. Predation is dependent on morphological and behavioral novelties, involving the formation of teeth-like denticles and a self-recognition mechanism [14][15][16][17].…”

Section: Introductionmentioning

confidence: 99%

Bacterial vitamin B12 production enhances nematode predatory behavior

et al. 2020

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Although the microbiota is known to affect host development, metabolism, and immunity, its impact on host behavior is only beginning to be understood. In order to better characterize behavior modulation by host-associated microorganisms, we investigated how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. This nematode is a predator that feeds on the larvae of other nematodes, including Caenorhabditis elegans. By growing P. pacificus on different bacteria and testing their ability to kill C. elegans, we reveal large differences in killing efficiencies, with a Novosphingobium species showing the strongest enhancement. This enhanced killing was not accompanied by an increase in feeding, which is a phenomenon known as surplus killing, whereby predators kill more prey than necessary for sustenance. Our RNA-seq data demonstrate widespread metabolic rewiring upon exposure to Novosphingobium, which facilitated screening of bacterial mutants with altered transcriptional responses. We identified bacterial production of vitamin B 12 as an important cause of such enhanced predatory behavior. Although vitamin B 12 is an essential cofactor for detoxification and metabolite biosynthesis, shown previously to accelerate development in C. elegans, supplementation with this enzyme cofactor amplified surplus killing in P. pacificus, whereas mutants in vitamin B 12 -dependent pathways reduced surplus killing. By demonstrating that production of vitamin B 12 by hostassociated microbiota can affect complex host behaviors, we reveal new connections between animal diet, microbiota, and nervous system.

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Section: Introductionmentioning

confidence: 99%

Bacterial vitamin B12 production enhances nematode predatory behavior

et al. 2020

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“…Mouth-form phenotyping was performed as previously reported 6,33 . In brief, axenic worm eggs were obtained by treating healthy gravid P. pacificus adults with alkaline hypochlorite, which were subsequently maintained on the test bacteria strains or mutants for at least two generations.…”

Section: Mouth-form Phenotypingmentioning

confidence: 99%

“…We used two types of predation assays as described below. Corpse assays facilitated rapid quantification of predatory behavior and were conducted as previously described 6,10,33 . Briefly, in order to generate substantial C. elegans larvae for use as prey, cultures were maintained on E. coli OP50 bacteria until freshly starved resulting in an abundance of young larvae.…”

Section: Predation Assaysmentioning

confidence: 99%

“…After recovery, the predatory animal was directly observed under a light stereomicroscope for 10 min and the number of bites, successful bites and feeding events quantified. "Bites" were characterized by a switch to the slower predatory pharyngeal pumping rhythms previously described 6,33 coinciding with a restriction in movement of the prey. "Successful bites" were characterized by successful rupturing of the prey cuticle resulting in sufficient damage to cause the innards to leak from the wound.…”

Section: Corpse Assaysmentioning

confidence: 99%

“…Thus, the presence of vitamin B12 might act through multiple downstream factors, but how it stimulates these effects has yet to be discovered. Importantly however, several neural circuits and neurotransmitter systems of P. pacificus have been investigated 6,[32][33][34] . Therefore, future studies can reveal the cellular and molecular foci of vitamin B12-dependence and the influence of the microbiota on nematode predatory behaviors.…”

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Bacterial derived vitamin B12 enhances predatory behaviors in nematodes

Akduman

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Roeseler

et al. 2019

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1 1 2 3 4 5 6 7 8 9 10The microbiome is known to affect host development, metabolism and immunity, however, its impact on behaviors is only beginning to be understood. Here, we investigate how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. P. pacificus is a predator feeding on the larvae of other nematodes including Caenorhabditis elegans. Growing P. pacificus on different bacteria and testing their ability to kill C. elegans reveals drastic differences in killing efficiencies with a Novosphingobium species showing the strongest enhancement. Strikingly, increased killing was not accompanied by an increase in feeding, a phenomenon known as surplus-killing whereby predators kill more prey than necessary for sustenance. RNA-seq revealed widespread metabolic rewiring upon exposure to Novosphingobium, which facilitated the screening for bacterial mutants leading to an altered transcriptional response. This identified bacterial derived vitamin B12 as a major micronutrient enhancing predatory behaviors. Vitamin B12 is an essential cofactor for detoxification and metabolite biosynthesis and has previously been shown to accelerate development in C. elegans. In P. pacificus vitamin B12 supplementation amplified, whereas mutants in vitamin B12-dependent pathways reduced surplus-killing. This demonstrates that bacterial vitamin B12 affects complex behaviors and thus establishes a connection between microbial diet and the nervous system.The microbiome is considered a fundamental aspect of a host's biology and is known to provide developmental cues, influence metabolism and alter immunity 1-3 . However, the microbiome constitutes a complex network of microorganisms and disentangling specific interactions and effects at a mechanistic level is challenging. Bacterialfeeding nematodes constitute a highly attractive system to study the influence of the microbiome because specific interactions can be investigated in monoxenic cultures where the microbiome and diet are indistinguishable from one another and easily controlled. To study the effect of bacteria on behavior we investigate the nematode model organism Pristionchus pacificus that exhibits a particular complex behavior unknown from C. elegans. In general, P. pacificus is an omnivorous nematode that can grow on bacteria, fungi and it can predate on other nematodes 4-6 . Predation is dependent on morphological and behavioral novelties, involving the formation of teeth-like denticles and a self-recognition mechanism 7-10 . The ability to form teeth-like denticles is an example of developmental plasticity with two discrete mouth-forms 11 .The stenostomatous morph has a single blunt tooth, whereas the eurystomatous morph has two large teeth with only the latter capable of predation ( Fig. 1A and B) 7 .Predation may confer a selective advantage in certain environmental settings with previous studies indicating that different culture conditions, including microbial diet, are able to modulate the ratio of the two mouth forms 12,13 . Further...

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Screening for CRISPR/Cas9-induced mutations using a co-injection marker in the nematode Pristionchus pacificus

et al. 2020

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CRISPR/Cas9 genome editing methods are used to reveal functions of genes and molecular mechanisms underlying biological processes in many species, including nematodes. In evolutionary biology, the nematode Pristionchus pacificus is a satellite model and has been used to understand interesting phenomena such as phenotypic plasticity and self-recognition. In P. pacificus, CRISPR/Cas9-mediated mutations are induced by microinjecting a guide RNA (gRNA) and Cas9 protein into the gonads. However, mutant screening is laborious and time-consuming due to the absence of visual markers. In this study, we established a Co-CRISPR strategy by using a dominant roller marker in P. pacificus. We found that heterozygous mutations in Ppa-prl-1 induced the roller phenotype, which can be used as an injection marker. After the co-injection of Ppa-prl-1 gRNA, target gRNA, and the Cas9 protein, roller progeny and their siblings were examined using the Heteroduplex Mobility Assay and DNA sequencing. We found that some of the roller and non-roller siblings had mutations at the target site. We used varying Cas9 concentrations and found that a higher concentration of Cas9 did not increase genome-editing events. The Co-CRISPR strategy promotes the screening for genome-editing events and will facilitate the development of new genome-editing methods in P. pacificus.

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Serotonin Drives Predatory Feeding Behavior via Synchronous Feeding Rhythms in the Nematode Pristionchus pacificus

Cited by 30 publications

References 33 publications

Bacterial vitamin B12 production enhances nematode predatory behavior

Bacterial vitamin B12 production enhances nematode predatory behavior

Bacterial derived vitamin B12 enhances predatory behaviors in nematodes

Screening for CRISPR/Cas9-induced mutations using a co-injection marker in the nematode Pristionchus pacificus

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