scholarly journals C. elegans pathogenic learning confers multigenerational pathogen avoidance

2018 ◽  
Author(s):  
Rebecca S. Moore ◽  
Rachel Kaletsky ◽  
Coleen T. Murphy

AbstractThe ability to pass on learned information to progeny could present an evolutionary advantage for many generations. While apparently evolutionarily conserved1–12, transgenerational epigenetic inheritance (TEI) is not well understood at the molecular or behavioral levels. Here we describe our discovery that C. elegans can pass on a learned pathogenic avoidance behavior to their progeny for several generations through epigenetic mechanisms. Although worms are initially attracted to the gram-negative bacteria P. aeruginosa (PA14)13, they can learn to avoid this pathogen13. We found that prolonged PA14 exposure results in transmission of avoidance behavior to progeny that have themselves never been exposed to PA14, and this behavior persists through the fourth generation. This form of transgenerational inheritance of bacterial avoidance is specific to pathogenic P. aeruginosa, requires physical contact and infection, and is distinct from CREB-dependent long-term associative memory and larval imprinting. The TGF-β ligand daf-7, whose expression increases in the ASJ upon initial exposure to PA1414, is highly expressed in the ASI neurons of progeny of trained mothers until the fourth generation, correlating with transgenerational avoidance behavior. Mutants of histone modifiers and small RNA mediators display defects in naïve PA14 attraction and aversive learning. By contrast, the germline-expressed PRG-1/Piwi homolog15 is specifically required for transgenerational inheritance of avoidance behavior. Our results demonstrate a novel and natural paradigm of TEI that may optimize progeny decisions and subsequent survival in the face of changing environmental conditions.

Author(s):  
Carola Petersen ◽  
Barbara Pees ◽  
Christina Martínez Christophersen ◽  
Matthias Leippe

In comparison with the standard monoxenic maintenance in the laboratory, rearing the nematode Caenorhabditis elegans on its natural microbiota improves its fitness and immunity against pathogens. Although C. elegans is known to exhibit choice behavior and pathogen avoidance behavior, little is known about whether C. elegans actively chooses its (beneficial) microbiota and whether the microbiota influences worm behavior. We examined eleven natural C. elegans isolates in a multiple-choice experiment for their choice behavior toward four natural microbiota bacteria and found that microbiota choice varied among C. elegans isolates. The natural C. elegans isolate MY2079 changed its choice behavior toward microbiota isolate Ochrobactrum vermis MYb71 in both multiple-choice and binary-choice experiments, in particular on proliferating bacteria: O. vermis MYb71 was chosen less than other microbiota bacteria or OP50, but only after preconditioning with MYb71. Examining escape behavior and worm fitness on MYb71, we ruled out pathogenicity of MYb71 and consequently learned pathogen avoidance behavior as the main driver of the behavioral change toward MYb71. The change in behavior of C. elegans MY2079 toward microbiota bacterium MYb71 demonstrates how the microbiota influences the worm’s choice. These results might give a baseline for future research on host–microbiota interaction in the C. elegans model.


2002 ◽  
Vol 69 ◽  
pp. 117-134 ◽  
Author(s):  
Stuart M. Haslam ◽  
David Gems ◽  
Howard R. Morris ◽  
Anne Dell

There is no doubt that the immense amount of information that is being generated by the initial sequencing and secondary interrogation of various genomes will change the face of glycobiological research. However, a major area of concern is that detailed structural knowledge of the ultimate products of genes that are identified as being involved in glycoconjugate biosynthesis is still limited. This is illustrated clearly by the nematode worm Caenorhabditis elegans, which was the first multicellular organism to have its entire genome sequenced. To date, only limited structural data on the glycosylated molecules of this organism have been reported. Our laboratory is addressing this problem by performing detailed MS structural characterization of the N-linked glycans of C. elegans; high-mannose structures dominate, with only minor amounts of complex-type structures. Novel, highly fucosylated truncated structures are also present which are difucosylated on the proximal N-acetylglucosamine of the chitobiose core as well as containing unusual Fucα1–2Gal1–2Man as peripheral structures. The implications of these results in terms of the identification of ligands for genomically predicted lectins and potential glycosyltransferases are discussed in this chapter. Current knowledge on the glycomes of other model organisms such as Dictyostelium discoideum, Saccharomyces cerevisiae and Drosophila melanogaster is also discussed briefly.


2020 ◽  
Vol 48 (3) ◽  
pp. 1019-1034 ◽  
Author(s):  
Rachel M. Woodhouse ◽  
Alyson Ashe

Gene regulatory information can be inherited between generations in a phenomenon termed transgenerational epigenetic inheritance (TEI). While examples of TEI in many animals accumulate, the nematode Caenorhabditis elegans has proven particularly useful in investigating the underlying molecular mechanisms of this phenomenon. In C. elegans and other animals, the modification of histone proteins has emerged as a potential carrier and effector of transgenerational epigenetic information. In this review, we explore the contribution of histone modifications to TEI in C. elegans. We describe the role of repressive histone marks, histone methyltransferases, and associated chromatin factors in heritable gene silencing, and discuss recent developments and unanswered questions in how these factors integrate with other known TEI mechanisms. We also review the transgenerational effects of the manipulation of histone modifications on germline health and longevity.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Ippei Kotera ◽  
Nhat Anh Tran ◽  
Donald Fu ◽  
Jimmy HJ Kim ◽  
Jarlath Byrne Rodgers ◽  
...  

Understanding neural functions inevitably involves arguments traversing multiple levels of hierarchy in biological systems. However, finding new components or mechanisms of such systems is extremely time-consuming due to the low efficiency of currently available functional screening techniques. To overcome such obstacles, we utilize pan-neuronal calcium imaging to broadly screen the activity of the C. elegans nervous system in response to thermal stimuli. A single pass of the screening procedure can identify much of the previously reported thermosensory circuitry as well as identify several unreported thermosensory neurons. Among the newly discovered neural functions, we investigated in detail the role of the AWCOFF neuron in thermal nociception. Combining functional calcium imaging and behavioral assays, we show that AWCOFF is essential for avoidance behavior following noxious heat stimulation by modifying the forward-to-reversal behavioral transition rate. We also show that the AWCOFF signals adapt to repeated noxious thermal stimuli and quantify the corresponding behavioral adaptation.


2018 ◽  
Author(s):  
Yi Jin Liew ◽  
Emily J. Howells ◽  
Xin Wang ◽  
Craig T. Michell ◽  
John A. Burt ◽  
...  

MainThe notion that intergenerational or transgenerational inheritance operates solely through genetic means is slowly being eroded: epigenetic mechanisms have been shown to induce heritable changes in gene activity in plants1,2and metazoans1,3. Inheritance of DNA methylation provides a potential pathway for environmentally induced phenotypes to contribute to evolution of species and populations1–4. However, in basal metazoans, it is unknown whether inheritance of CpG methylation patterns occurs across the genome (as in plants) or as rare exceptions (as in mammals)4. Here, we demonstrate genome-wide intergenerational transmission of CpG methylation patterns from parents to sperm and larvae in a reef-building coral. We also show variation in hypermethylated genes in corals from distinct environments, indicative of responses to variations in temperature and salinity. These findings support a role of DNA methylation in the transgenerational inheritance of traits in corals, which may extend to enhancing their capacity to adapt to climate change.


Author(s):  
David E. Henley ◽  
Joey M. Kaye ◽  
Stafford L. Lightman

In the face of any threat or challenge, either real or perceived, an organism must mount a series of coordinated and specific hormonal, autonomic, immune, and behavioural responses that allow it to either escape or adapt (1–3). To be successful, the characteristics and intensity of the response must match that posed by the threat itself and should last no longer than is necessary. A response that is either inadequate or excessive in terms of its specificity, intensity or duration may result in one or more of a multitude of psychological or physical pathologies (2–5). This concept of threat and the organism’s response to it is frequently recognized and understood as ‘stress’ but is so diverse that it lacks a universally accepted definition (2) and thus is difficult to investigate or study (6). In the early 1900s, Walter Cannon introduced the concept of homoeostasis (4)—an ideal steady state for all physiological processes. Stress has been defined as the state where this ideal is threatened. More easily appreciated, however, are those factors, both intrinsic and extrinsic, which represent a challenge to homoeostasis (termed stressors) and the complex physiological, hormonal, and behavioural responses that occur to restore the balance, the stress response (1). The importance of endocrine systems in this stress response was emphasized by Hans Selye (7), who described the need for multiple, integrated systems to respond in a coordinated fashion following exposure to a particular stressor. Nonspecific activation of the hypothalamic–pituitary–adrenal (HPA) and sympatho-adrenomedullary (SAM) axes occurred following initial exposure to a noxious stimulus. Continued exposure to the same agent has been shown to have lasting and damaging effects on various endocrine, immune, and other systems, although recovery from this state was possible provided the stress was terminated (7). In addition to various noxious agents, numerous potential stressors exist including exertion, physical extremes, trauma, injury, and psychological stress. Indeed, psychological stressors are some of the most potent stimuli of the endocrine stress response particularly when they involve elements of novelty, uncertainty, and unpredictability. This has been highlighted by the observation that anticipating an event can be as potent an activator of the stress response as the event itself (7).


Author(s):  
Philip Joosten ◽  
Alexia Van Cleven ◽  
Steven Sarrazin ◽  
Dominique Paepe ◽  
An De Sutter ◽  
...  

Contact and interactions between owners and their pets may have beneficial physical and social effects on people, but may also facilitate the transmission of zoonotic agents and resistant bacteria. To estimate the risk of these contacts, more information regarding the frequency and intensity of this physical contact is required. Therefore, an online survey was conducted among pet owners resulting in 701 completed questionnaires. Questions regarding the interactions between dogs and owners were linked with a score from 1 (limited interactions) to 3 (highly intense interactions). After scoring these self-reported interactions, a contact intensity score was calculated for each respondent by summing up the different allocated scores from all questions. This contact intensity score was used to identify predictors of more intense contact based on a multivariable linear regression model. Interactions between dogs and their owners were widespread (e.g., 85.3% of the dogs licked their owner’s hand) and intense (e.g., 49.3% of owners reported being licked in the face). The gender, age, and place of residence (city, village, or countryside) of the respondent, together with the size and age of the dog, were significantly associated with the contact intensity score in the multivariable model. On average, female respondents younger than 65 years who lived in the city and had a small young dog had the most intense contact with it. Further research is necessary to evaluate the risk of these interactions in light of zoonotic and antimicrobial resistance transfer.


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