Boehnisch C., Wong D., Habig M., Isermann K., Michiels N. K., et al., 2011. Yet, even for C. elegans, it remains an exciting challenge to find out how frequent potentially conflicting malehermaphrodite interactions really occur in nature and to what extent they have shaped C. elegans life history evolution. Interestingly, the characterized QTL consisted of polymorphic G protein-coupled chemoreceptors (Greene et al. Thomas C. G., Li R., Smith H. E., Woodruff G. C., Oliver B., et al., 2012. 2008; Shi and Murphy 2014; Palopoli et al. (A) Infected C. elegans adult on an agar plate. Identification of attractive odorants released by preferred - PLOS Can bacteria that survive the pharyngeal grinder of the nematode be later digested in the gut? Absence of PEEL-1 (not shown) always results in zygote survival. Decaestecker E., Gaba S., Raeymaekers J. 2012). Rapid increase in frequency of gene copy-number variants during experimental evolution in. 2013). Bar, 1 cm. While observing predation of C. elegans in the wild context is a challenge, testing whether an organism preys on C. elegans under artificial laboratory conditions is not necessarily relevant. This has been particularly well-documented for interactions of host organisms with their coevolving parasites and pathogens (Woolhouse et al. Cook D. E., Zdraljevic S., Tanny R. E., Seo B., Riccardi D. D., et al., 2016. Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. MB) enhances population growth relative to E. coli OP50 (see horizontal axes) under stress conditions such as nutrient-poor media or high temperatures (left panels), and also different salt conditions (right columns). From an evolutionary point of view, C. elegans is a suitable model for the identification of the molecular processes involved in pathogenic and commensal Biology and genome of a newly discovered sibling species of (2008), reprinted with permission from AAAS. Pradel E., Zhang Y., Pujol N., Matsuyama T., Bargmann C. I., et al., 2007. Oomycetes include mostly plant-infecting species, such as Phytophthora infestans, which causes the potato blight disease. 2016). A recent study demonstrated nematode-mediated dispersal of E. coli, which resulted in a growth advantage for the bacteria on the new substrate patches and, most impressively, a subsequent increase in population growth of C. elegans (Thutupalli et al. Franz C. J., Zhao G., Flix M.-A., Wang D., 2012. (C) Formation of spores in the sporangia. The first natural pathogens and parasites of C. elegans were described in 2008 and 2011 (Troemel et al. The relationship of C. elegans to food around it has been studied in various ways, but so far not using the recently isolated bacteria naturally found with C. elegans. Host biology in light of the microbiome: ten principles of holobionts and hologenomes. In the case of C. elegans, more details on the specificity of the interaction would now require specially designed studies, such as life history assays on the host or collection of dead hosts from the wild (beyond one anecdotal report in Barrire and Flix 2007). 2015). Diverse and potentially manipulative signalling with ascarosides in the model nematode. Orsay virus utilizes ribosomal frameshifting to express a novel protein that is incorporated into virions. (B) Schematic depiction of the life cycle of N. parisii in C. elegans. Phylogenetics and evolution of nematode-trapping fungi (Orbiliales) estimated from nuclear and protein coding genes. Petersen C., Dirksen P., Prahl S., Strathmann E. A., Schulenburg H., 2014. The Gram-negative opportunistic pathogen S. marcescens is common in diverse environments, and an isolate showing the ability to swarm was previously found together with C. elegans in a compost sample in France (M.-A. The arrowhead indicates collembola. Watson E., MacNeil L. T., Ritter A. D., Yilmaz L. S., Rosebrock A. P., et al., 2014. Bellier A., Chen C.-S., Kao C.-Y., Cinar H. N., Aroian R. V., 2009. 2011), they are likely able to better survive on animals that provide a more humid environment, such as isopods and the various molluscs. Evolution of host innate defence: insights from. Ghosh R., Andersen E. C., Shapiro J. Additional factors such as hermaphrodite receptivity may further contribute to variation in the proportion of males. Yang W., Dierking K., Esser D., Tholey A., Leippe M., et al., 2015. C. elegans presents a low level of molecular diversity, which may be explained by its selfing mode of reproduction. Flix M.-A., Ashe A., Piffaretti J., Wu G., Nuez I., et al., 2011. Lim M.-P., Firdaus-Raih M., Nathan S., 2016. WebCaenorhabditis elegans is a small nematode worm, about 1mm long, which we use as a model organism. Virk B., Jia J., Maynard C. A., Raimundo A., Lefebvre J., et al., 2016. 1999; Mahajan-Miklos et al. (B) Reproduced from Szumowski et al. Introduction. Nevertheless, matings do occur in the wild, leading to the occasional presence of heterozygote individuals and genetic exchange (Barrire and Flix 2005, 2007; Haber et al. Caenorhabditis elegans - Latest research and news | Nature 2008). 2016) (Figure 6A). 2008). 3.1 Finding Suitable Habitats and Substrate Samples. The third one, L. celer CBX151/Verde 1, coats the whole surface of the nematode (Figure 11A). It feeds on microorganisms like The nematode also responds positively to specific volatile organic compounds, such as 2-heptanone, of B. nematocida (Niu et al. 2010, 2011, 2012, Masri et al. How do we best analyze such environmental contributions under laboratory conditions? Bar, 10 m. 2008). Farslow J. C., Lipinski K. J., Packard L. B., Edgley M. L., Taylor J., et al., 2015. Caenorhabditis Elegans - an overview | ScienceDirect Topics Balla K. M., Andersen E. C., Kruglyak L., Troemel E. R., 2015. Consistent with the above study (Dirksen et al. Zhang F., Peng D., Cheng C., Zhou W., Ju S., et al., 2016. The pathogen may induce harm by disrupting cellular integrity or cellular and physiological homeostasis. 2010; C. Zhang et al. C. elegans | Mair Lab | Harvard T.H. Chan School of Public 2016), and also food bacteria (Bendesky et al. Another influential type of intraspecific interaction is found among the two sexes. 2011; Andersen et al. Table 1. 2016b). In these last stages of infection, fungal hyphae bearing spores exit from the dead nematodes. Hsueh Y.-P., Mahanti P., Schroeder F. C., Sternberg P. W., 2013. WebThe spontaneous micro mutant in C. briggsae corresponds to a common class of mutants found in C. elegans and other rhabditids, now called dumpy (abbreviated dpy) following Brenner (1974). It is even possible that C. elegans may thereby harm slugs. 2016), whereas the other exposed the canonical laboratory strain N2 to defined substrates under controlled conditions, followed by microbiome characterizations (Berg et al. A third Nematocida species with a different tissue tropism has been found recently in a wild-caught C. elegans, and named N. displodere (Luallen et al. The nutritional requirements of Caenorhabditis elegans Die Nematoden der Regenwrmer und aasbesuchenden Kfer. Host-parasite local adaptation after experimental coevolution of. Szumowski S. C., Estes K. A., Popovich J. J., Botts M. R., Sek G., et al., 2016. Is the 16S rDNA in the gut of C. elegans that of the food or mostly that of live bacteria that will not be digested? Read D. S., Sheppard S. K., Bruford M. W., Glen D. M., Symondson W. O. C., 2006. 2016; Samuel et al. Haber M., Schngel M., Putz A., Mller S., Hasert B., et al., 2005. Individual microsporidia taxa may thus be able to infect closely related species, but not necessarily all rhabditids. Population dynamics and habitat sharing of natural populations of. WebCaenorhabditis elegans are often called C. elegans or simply 'the worm' because they are a model species. Jiang H., Franz C. J., Wu G., Renshaw H., Zhao G., et al., 2014. 2016). The latter include food bacteria (as examples members of the genera Acetobacter, Gluconobacter, and Enterobacter), then pathogens and parasites (e.g., microsporidia, the Orsay virus, the fungus D. coniospora, and the bacteria P. aeruginosa, B. thuringiensis, and Leucobacter sp. Kirienko N. V., Kirienko D. R., Larkins-Ford J., Whlby C., Ruvkun G., et al., 2013. In this last stage of infection, the oomycete forms in the host body spherical multinucleate structures called sporangia. C Food and metabolic signalling defects in a. Szewczyk N. J., Kozak E., Conley C. A., 2003. OP50. Molecular detection of predation by soil micro-arthropods on nematodes. 2008; Anderson et al. The interaction between C. elegans and B. thuringiensis was established as a model for experimental evolution, to study the dynamics of hostpathogen coevolution. This may be a consequence of genetic adaptation of C. elegans to its microbial environment, possibly based on its behavioral choice, grinder properties, gut environment, or defecation efficacy. In one case (green dot), zeel-1 is active, but there is not paternal killing through peel-1. Another study was based on an evolution experiment, which favored the emergence of infectious P. aeruginosa varieties that supported proliferating C. elegans populations (Jansen et al. 2013; Lim et al. 2010; Pukkila-Worley and Ausubel 2012; Kim and Ewbank 2015). The aim of this review is to summarize our current understanding of the naturally occurring interactions of C. elegans with other organisms, ranging from conspecifics to interactions with other species (Figure 1). A., Parrish R. C., Lively C. M., 2011. Of those tested for their effect on C. elegans, some strains strongly diminish brood size and are thus potential pathogens, for example some (not all) members of Pseudomonas (MYb193), Microbacterium (MYb45 and MYb50), Bacillus (MYb78 and MYb56), Chryseobacterium (MYb7 and MYb120), Arthrobacter (MYb27), Rhodococcus (MYb53), Leuconostoc (MYb83), and Sphingobacterium (MYb181 and MYb210) (Dirksen et al. These are some of the many questions that need to be addressed in future research. Lebrigand K., He L. D., Thakur N., Arguel M.-J., Polanowska J., et al., 2016. Goranson N. C., Ebersole J. P., Brault S., 2005. This model infection system was explored in numerous studies to dissect the molecular basis of the nematodes immune defense system. It is so far unclear whether dauer larvae may carry bacteria, but feeding stages certainly do. In this context, it may be speculated that access to these environmental nutrients may be mediated by bacterial members of the nematodes microbiome. 1977). This nematode is particularly abundant in microbe-rich environments, especially rotting plant matter such as decomposing fruits and stems. Isolating Caenorhabditis elegans from the Natural Habitat They have also been implicated in human cancers. 45). Volkers R. J., Snoek L. B., van Hellenberg Hubar C. J., Coopman R., Chen W., et al., 2013. 2015). 2011; Nakad et al. Besides potentially providing a substrate for bacterial growth, C. elegans may also disperse micro-organisms. GATA transcription factor as a likely key regulator of the. In principle, such vertical transmission may occur through eggs (i.e., transovarial transmission, so far not seen in C. elegans), through transfer to the developing offspring in the uterus (enhanced when larvae hatch inside their mothers, an essential feature for symbiont transmission in Heterorhabditis) (Ciche et al. Moreover, analysis of small molecular metabolites produced by C. elegans suggests a modular and flexible assembly of molecular signals that not only function as regulators of development, life span, and dauer formation (see above), but also aggregation and malehermaphrodite interactions (i.e., sex pheromone; Ludewig and Schroeder 2013; Schroeder 2015; Dong et al. Symbiotic digestion of lignocellulose in termite guts. During the 20th century, a handful of studies repeatedly isolated C. elegans from nature and characterized specific aspects of its ecology, for example its interaction Males can be produced by hermaphrodites as a consequence of X chromosome nondisjunction or as crossprogeny of a male and a hermaphrodite. 2016). We describe a new type of collective behavior in C. elegans nematodes, aggregation of starved L1 larvae. Altered bacterial metabolism, not coenzyme Q content, is responsible for the lifespan extension in. This lack of interest changed 10 yr ago. Bacteria do not provide all nutrients required for C. elegans, and specifically this nematode requires an external sterol source (Hieb and Rothstein 1968; Lu et al. 2009; Kao et al. Smaller size bacteria tend to be better food (Avery and Shtonda 2003). The composition of the gut community then depends on the interaction between both host and microbe properties: on the host side on the foraging and feeding behaviors and the properties of the gut lumen; and on the microbe side, on the ability to pass the pharyngeal grinder and to persist in the gut without the population being entirely digested or expelled live by defecation. The interest in C. elegans natural populations has especially gained momentum since 2005, when several articles on its natural distribution and population genetic characteristics were published (Barrire and Flix 2005; Haber et al. Nematode-eating collembola have also been observed in samples with C. elegans. The natural habitat of C. elegans contains many bacterial species; about a third of these are in the genus Pseudomonas, and can be beneficial or detrimental 1. Schulenburg H., Kurtz J., Moret Y., Siva-Jothy M. T., 2009. Importantly, C. elegans-associated communities from the two very distinct study approaches are highly similar, including enrichment of eight particular families across the two studies, such as Enterobacteriaceae, Pseudomonaceae, Xanthomonadaceae, Comamonadaceae, Sphingomonadaceae, Sphingobacteriaceae, Weeksellaceae, and Flavobacteriaceae (Zhang et al. Lee S.-H., Wong R.-R., Chin C.-Y., Lim T.-Y., Eng S.-A., et al., 2013. C. elegans may, thus, possess a hemerophilous (human-associated) lifestyle, as already described for various bird species or mammals (e.g., house sparrow, common pigeon, and house mouse, etc. Yet, as explained below, several lines of evidence suggest them to be influential. 2011; Franz et al. (2012) identified a long-term polymorphism in the chloride channel subunit gene glc-1 that explains resistance to the antihelminthic avermectin. In this case, the nematode appears compromised in its ability to feed and process nutrients, leading to reduced progeny production (Flix and Duveau 2012). ), C. remanei (C.r. (A) From Petersen et al. Quantitative genetic analysis of life-history traits of. C. elegans eats bacteria and grows in various types of bacteria-rich rotting plant material. 2007), while ASP-1-mediated necrosis enhances susceptibility to the toxin Cry6Aa (F. Zhang et al. Interestingly, the microsporidian proteins that are exposed to the host cytoplasm or nucleus tend to bear signal peptides or transmembrane domains and belong to large and/or fast-evolving, species-specific gene families (Reinke et al. Overview of biotic interactions of C. elegans. connectomes The mature spores are surrounded by an additional membrane and routed through a vesicular pathway, recruiting RAB-11 and an actin coat, until they exit to the gut lumen (Szumowski et al. For nematode-harming fungi, a rather arbitrary frontier between predation and pathogens/parasites is usually set depending on the size of the relevant fungal life stage relative to the worm: hyphae for predators (Competitors and Predators) and spores for pathogens/parasites (here). Adaptive value of a predatory mouth-form in a dimorphic nematode. 2016). 2002; W. Yang et al. The major routes of infection are through the intestine and the epidermis. Pujol N., Link E. M., Liu L. X., Kurz C. L., Alloing G., et al., 2001. In the different substrate samples, sequences from the bacterial phyla Proteobacteria (mostly - and -Proteobacteria), Bacteroidetes, Firmicutes, and Actinobacteria were most common. The arrowhead indicates an isopod. (2013)]. Figure 9, panels D and E, shows the rescue of the wild isolate JU1580 by an intact drh-1(N2) transgene. Moreover, C. elegans can respond by activating its immune system, especially through the p38 MAPK pathway, the GATA transcription factor ELT-2, the insulin-like signaling cascade, and the hypoxia response (Kim et al. 2014, 2015b; Frzal and Flix 2015; Cook et al. On the one hand, competition occurs within growing populations, especially when density increases and nutrient availability decreases. 2016), while resistance is influenced by lysozymes and C type lectins (Mallo et al. Although the majority of worms in the intestines were dauers, some non-dauers were also repeatedly isolated, suggesting survival of other stages in slug intestines and possibly their reproduction in this environment. Indeed, so far there is no indication of a vertically transmitted symbiont in C. elegans (except for genome-encoded retrotransposon sequences that can assemble capsids in the germline of some isolates; Dennis et al. Nematode-trapping fungi eavesdrop on nematode pheromones. Some C. elegans larvae escape using active mechanosensation and suppression of lateral head movements while backing (Maguire et al. The replication cycle of RNA viruses includes a double-stranded stage, to which C. elegans may respond by initiating a small RNA cascade that degrades the viral RNAs (Flix et al. However, an overlap occurred in the fall, and many samples in rotting stems in woods also contained both species in feeding stages, indicating possible competition (Flix and Duveau 2012). 2017). The latter result suggests that some specificity of colonization takes place. 3.1 Finding Suitable Habitats and Substrate Samples. (D and E) Reprinted from Ashe et al. 2013; Clark and Hodgkin 2015). Others induced expression of C. elegans genes usually activated by other stresses or pathogens, and at least some of these bacteria appeared pathogenic, because their effect could not be rescued by good food (Liu et al. These two genes define a toxinantitoxin system at the same genetic locus. A survey in Scotland isolated C. elegans from isopods such as Porcellio scaber and Po. Chandler J. Toward a synthesis of developmental biology with evolutionary theory and ecology. These two genes are subject to balancing selection in natural C. elegans populations (Greene et al. C Further details on the etiology and genetics of C. elegansmicrosporidia interactions have been nicely summarized elsewhere (Balla and Troemel 2013; Bakowski et al. As we will discuss below, the natural history of C. elegans is much less studied than is the case for other model organisms, and its ecological significance is largely unknown, though nematodes are found in terrestrial and aquatic ecosystems (Brusca, 2016; Kiontke et al., 2011). 2010). 2012), and (iii) iron-dependent, hypoxia-mediated killing in liquid medium (Kirienko et al. Meisel J. D., Panda O., Mahanti P., Schroeder F. C., Kim D. H., 2014. 2016), the results demonstrated a worm-specific microbiome that was distinct from the corresponding substrates and that was highly similar, even if assembled from different substrates (e.g., characterized by different fruits added to the soil). the contents by NLM or the National Institutes of Health. A likely reason is that the species natural ecology is largely neglected across these studies. All figures from Dirksen et al. (C) Localization of C. elegans (dark gray) and C. remanei (light gray) in different slug body parts, based on 35 tested slugs in 2013 in North Germany, highlighting a high abundance of C. elegans in slug intestines. In analogy to the gut microbiomes of termites (Brune 2014; Peterson and Scharf 2016) or ruminants (Krause et al. As a consequence of these fast evolutionary dynamics, the microbial environment can impose continuously high selective pressures on C. elegans. 2014). C. elegans is most easily isolated from rotting fruits and stems, compost, and some invertebrates (see below Macroscopic Invertebrates as Possible Vectors or Hosts). C. elegans responds to Drechmeria infection by the secretion of antimicrobial peptides and other cellular responses that ameliorate its survival and reproduction capacity. WebThus C. elegans provides the researcher with the ideal compromise between complexity and tractability. Gravato-Nobre M. J., Stroud D., ORourke D., Darby C., Hodgkin J., 2011. They induce a local swelling of the anal region and harm the animal. are specialized predators (e.g., Mikola and Sulkova 2001), but have not been noted so far in samples with Caenorhabditis. To date, more than 40 microbes have been shown to be pathogenic to C. elegans, including bacteria, fungi, and viruses. In C. elegans, such natural polymorphisms have been studied for a variety of traits. Most nematode-trapping fungi belong to a clade in Orbiliomycetes (Li et al. Several of these bacteria are nevertheless likely to be relevant in the natural context, for example P. aeruginosa, Bacillus thuringiensis, and Serratia marcescens, for which there is some indication for coexistence with C. elegans and which we describe in more detail below. 2015c), which may possibly be used as a completely different type of bacteria-rich substrate (see more details in Macroscopic Invertebrates as Possible Vectors or Hosts). Ciche T. A., Kim K. S., Kaufmann-Daszczuk B., Nguyen K. C., Hall D. H., 2008. Finally, dauers crawl up the fruiting bodies and nictate, helping in their own dispersal. A similar kind of relationship is further conceivable for snail species, which in some cases were also found to harbor C. elegans feeding stages (Flix and Duveau 2012). Detection and avoidance of a natural product from the pathogenic bacterium. is supported by grants from the German Science Foundation within the Collaborative Research Center 1182 on the origin and function of metaorganisms (projects A1.1 and A4.3). 2016), providing a valuable resource for studying the genetics of interacting pathogen and host molecules. To test the effect on C. elegans of these naturally associated bacteria, a culture collection of 565 bacteria was established from the diverse samples. (B) Proportion of bacterial strains of a particular genus from the natural environment of C. elegans, which either have positive (orange color), intermediate (gray), or detrimental effect (blue) on worm life history. N. parisii slows down progeny production and severely reduces C. elegans progeny number. 2015). Species richness, distribution and genetic diversity of. 2016). The Orsay virus has, so far, only been found on rare occasions in C. elegans isolates of the region around Paris (L. Frzal and M.-A. 2007; Schulte et al. The effect of other more naturally encountered bacteria has hardly been studied (Jensen et al. Slowinski S. P., Morran L. T., Parrish R. C., II, Cui E. R., Bhattacharya A., et al., 2016. 2017). Sironi M., Cagliani R., Forni D., Clerici M., 2015. Many more pathogens are likely to be discovered in the future. Other biotic interactions may impose similar selective constraints, for example those involving predators or competitors (Cortez and Weitz 2014; Hiltunen and Becks 2014; Wilson 2014). Nematode-trapping fungi are diverse and overall the best studied predators of small nematodes like C. elegans (Drechsler 1941; Gray 1987; Zhang and Hyde 2016). Natural variation in a chloride channel subunit confers avermectin resistance in. Teotnio H., Manoel D., Phillips P. C., 2006. 2013), chemicals produced by C. elegans that also act in dauer induction (as mentioned above) and male attraction behavior (Ludewig and Schroeder 2013). (A) Infected C. elegans larvae on an agar plate. Full appreciation of this nematodes biology warrants further exploration of its natural environment and subsequent integration of this information into the well-established laboratory-based research approaches.
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