Environmental influence on Pristionchus pacificus mouth form through different culture methods

Werner, Michael S.; Sieriebriennikov, Bogdan; Loschko, Tobias; Namdeo, Suryesh; Lenuzzi, Maša; Dardiry, Mohannad; Renahan, Tess; Sharma, Devansh Raj; Sommer, Ralf J.

doi:10.1038/s41598-017-07455-7

Cited by 65 publications

(93 citation statements)

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“…4B-C). Since the necromenic lifestyle in P. pacificus shares high similarity with parasitism, we propose that there might be an exogenous ligand regulating L. marina development, morphology and behavior via animalanimal communications, similar to that in beetle and P. pacificus pair's relationship (Werner et al 2017).…”

Section: Transposable Elements In L Marinamentioning

confidence: 89%

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Xie

Zhang

Xue

et al. 2020

Preprint

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Nematodes play key roles in marine ecosystem. Although oceans cover 71% of the Earth's surface, none of marine model nematode has been reported. Here, we constructed the first inbred line of free-living marine nematode Litoditis marina, sequenced and assembled its genome. Furthermore, we successfully applied CRISPR/Cas9 genome editing in L. marina.Comparative genomics revealed that immunity and oxygen regulation genes are expanded, which is probably central to its sediment adaptation. While L. marina exhibits massive gene contractions in NHRs, chemoreceptors, xenobiotics detoxification and core histones, which could explain the more defined marine environment. Our experiments showed that dozens of H4 genes in Caenorhabditis elegans might contribute to its adaptation to the complex terrestrial environments, while two H4 genes in L. marina are involved in salinity stress adaptation. Additionally, ninety-two conserved genes appear to be positively selected in L. marina, which may underpin its osmotic, neuronal and epigenetic changes in the sea. With short generation time, highly inbred lines, and genomic resources, our report brings L. marina a promising marine animal model, and a unique satellite marine model to the wellknown biomedical model nematode C. elegans. This study will underpin ongoing work on animal functional genomics, environmental adaptation and developmental evolution. 4 marine nematodes have had their genomes sequenced and analysed (International Helminth Genomes Consortium 2019; Smythe et al. 2019; Weinstein et al. 2019). Oceans cover 71% of the Earth's surface, and represents almost 99% of available habitat, which are a key element for the existence and evolution of life (Robert 1999; Peng et al. 2020). In marine sediments, free-living nematodes abound both in numbers and in local species diversity, comprising about 80% of the abundance of meiofauna (Heip et al. 1985; Danovaro et al. 2010; Nascimento et al. 2012), they play a key role in the benthic food web and ecosystem. However, the study of marine nematodes is largely limited to taxonomy and ecology (De Meester et al. 2016; Derycke et al. 2016). Molecular mechanisms underlying their evolution, development regulation and adaptation mechanisms are rarely reported, and none of marine model nematode has been reported. The bacterivorous marine nematode Litoditis marina (Bastian, 1865) Sudhaus, 2011, formerly known as Rhabditis marina or Pellioditis marina, is found widely distributed in the littoral zone of coasts and estuaries of European, American, African and Asian countries, and play an important role in these marine ecosystems (Tietjen et al. 1970; Kito 1981; Houthoofd et al. 2003; Derycke et al. 2016). In addition, the embryonic cell lineage of L. marina has been reported by Houthoofd et al. (2003). In comparison with C. elegans, the overall L. marina lineage homology is 95.5%, whereas the fate homology is only 76.4%, and most of the differences in fate homology concern nervous, epidermal, and pharyngeal tissues, suggesting that L. marina wil...

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Section: Transposable Elements In L Marinamentioning

confidence: 89%

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Xie

Zhang

Xue

et al. 2020

Preprint

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“…These were then seeded in 6 x 10 mL 252 flasks with OP50 as described in Werner et al, 2017 33 . Then at 24, 48, or 72 hr time intervals, 253 supernatant was obtained by centriguation (>4,000 x g, 4°C for 10 minutes).…”

Section: Hplc-ms Sample Preparation For Normal Exo-metabolome and Timmentioning

confidence: 99%

“…Among the many environmental influences on mouth form 33 , population density and 209 starvation is perhaps the most ecologically relevant. Indeed they have been shown to affect 210 numerous P. pacificus strains 16,34 , but teasing apart these two factors has proven difficult.…”

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Adult influence on juvenile phenotypes by stage-specific pheromone production

Werner

Claaßen

Renahan

et al. 2018

Preprint

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1Animals and plants can predict decreasing food supplies by recognition of population density, 2 and respond by adjusting behavioral and morphological traits. Population density in nematodes 3 is detected through pheromones, influencing dormant (dauer) stage entry, and in some lineages 4 alternative mouth-form decision (bacterivorous vs. predatory). Whether age is a relevant 5 parameter in recognizing population density is not well understood. Here, we utilized the mouth-6 form plasticity of the model nematode Pristionchus pacificus and developmental pheromone 7 profiling to study potential parent:progeny communication. Surprisingly, we observed adult-8 specific production of molecules that induce the predatory morph, even though adult mouth 9 forms are no longer plastic. We introduce a novel dye-based method to differentiate populations 10 in mixed-generation cultures, and found adults, but not peers, influence developing juvenile 11 mouth forms. Finally, we applied a logistic growth model that demonstrates adults both lower 12 the population carrying capacity and decrease the time until resource depletion. In the 13 necromenic life cycle of P. pacificus, we view mouth-form plasticity as an alternative 'Malthusian 14 escape' strategy to dauer that responds to age-specific population densities. The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/291591 doi: bioRxiv preprint first posted online Mar. 29, 2018; Population density is an important ecological parameter that correlates with increased 26 competition for resources 1 . In addition to density-dependent selection 2 , which operates on 27 evolutionary time scales, some organisms can respond dynamically to population density by 28 phenotypic plasticity. For example, plants can sense crowding by detecting the ratio of red 29 (chlorophyll absorbing) to far red (non-absorbing) light, and respond by various shade-30 avoidance strategies including higher shoots 3 . Locusts undergo solitary to swarm (i.e. 31 gregarious) transition, and aphids can develop wings, both as a result of increased physical 32 mechanosensory contact [4][5][6] . Intriguingly, population density can also have transgenerational 33 effects. For example, adult crowding of the desert locust Schistocerca gregaria 7,8 and migratory 34 locust Locusta migratoria 9 also influences the egg size, number, and morphology of their 35 progeny, and high population densities of red squirrels elicit hormonal regulation in mothers to 36 influence faster developing offspring 10 . Nevertheless, while incorporating age into population 37 structures has significantly advanced density-dependent selection theory 11 , surprisingly little 38age-specific refinement has been incorporated into models of phenotypic plasticity, especially at 39 the mechanistic level. This is partly due to the competing challenges of (1) studying population 40 ecology in the laboratory, and (2) the paucity of laboratory model organisms that are suitable for 41 ecological studies. The model nematode ...

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“…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 . Furthermore, P. pacificus predation under laboratory conditions is also an example of a phenomenon known as surplus-killing behavior 6 .…”

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confidence: 96%

Bacterial derived vitamin B12 enhances predatory behaviors in nematodes

Akduman

Lightfoot

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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Environmental influence on Pristionchus pacificus mouth form through different culture methods

Cited by 65 publications

References 69 publications

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Establishment of a marine nematode model for animal functional genomics, environmental adaptation and developmental evolution

Adult influence on juvenile phenotypes by stage-specific pheromone production

Bacterial derived vitamin B12 enhances predatory behaviors in nematodes

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