Improving the odds of survival: transgenerational effects of infections

EMBO Molecular Medicine, Год журнала: 2025, Номер unknown

Опубликована: Янв. 22, 2025

Abstract Recent studies argue for a novel concept of the role chromatin as carrier epigenetic memory through cellular and organismal generations, defining coordinating gene activity states physiological functions. Environmental insults, such exposures to unhealthy diets, smoking, toxic compounds, infections, can epigenetically reprogram germ-line cells influence offspring phenotypes. This review focuses on intergenerational transgenerational inheritance in different plants, animal species humans, presenting up-to-date evidence arguments effects light Darwinian Lamarckian evolutionary theories. An overview changes induced by infection or other immune challenges is presented, how these changes, known epimutations, contribute shaping The mechanisms that mediate transmission alterations via germline are also discussed. Understanding relationship between environmental fluctuations, resistance, susceptibility diseases critical unraveling disease etiology adaptive evolution.

Язык: Английский

---

Interspecies relationships of natural amoebae and bacteria with C. elegans create environments propitious for multigenerational diapause

mSystems, Год журнала: 2025, Номер unknown

Опубликована: Март 20, 2025

ABSTRACT The molecular and physical communication within the microscopic world underpins entire web of life as we know it. However, how organisms, such bacteria, amoebae, nematodes—all ubiquitous—interact to sustain their ecological niches, particularly associations generate influence behavior, remains largely unknown. In this study, developed a framework examine long-term interactions between microbes animals. From soil samples collected in temperate, semi-arid climate, isolated culturable bacterial genera, including Comamonas , Stenotrophomonas Chryseobacterium Rhodococcus well amoeba, Tetramitus . This microbial ensemble was fed nematode C. elegans experiments spanning over 20 generations assess developmental rate, dauer entry, fertility, feeding behavior. Our findings reveal that nematodes create stable environment where no species are exhausted, enter diapause after several generations. We have termed phenomenon formation on naturally derived ensembles (DaFNE). DaFNE occurs across range optimal temperatures, from 15°C 25°C, is dependent nematode’s pheromone biosynthesis pathway. intensifies with each passing generation, exhibiting both strong intergenerational transgenerational effects. Moreover, RNA interference (RNAi) pathway—both systemic cell-autonomous—is essential for initiating DaFNE, while heritable RNAi effectors required its These indicate RNA-mediated plays critical role bacterially induced behaviors natural environments. IMPORTANCE Microscopic most abundant multicellular animals Earth, which implies they evolved highly successful relationships associated microbiota. little known about behavior influenced complex ecosystems multiple organisms interact. used four bacteria an amoeba ecosystem explore behavioral responses Caenorhabditis 8 week period. striking finding nematodes’ commitment form hibernation diapause. results suggest nature may frequently result partners. requires production pheromones, pathway, indicating microbiota play role. Interestingly, at higher fewer needed trigger suggesting mild increase temperature promote environments without causing stress

Язык: Английский

---

Reported transgenerational responses to Pseudomonas aeruginosa in Caenorhabditis elegans are not robust

eLife, Год журнала: 2025, Номер 13

Опубликована: Март 26, 2025

We report our attempt to replicate reports of transgenerational epigenetic inheritance in Caenorhabditis elegans . Multiple laboratories that C. adults and their F1 embryos exposed the pathogen Pseudomonas aeruginosa show aversion behavior increased daf-7/TGFβ reporter gene expression. However, results from one group persistence both through F4 generation. failed consistently detect either avoidance response or elevated daf-7 expression beyond confirmed dsRNA transport proteins SID-1 SID-2 are required for intergenerational (F1) avoidance, but not Reanalysis RNA seq data provides additional evidence this inherited PA14 may be mediated by small RNAs. The experimental methods well-described, source materials readily available, including samples reporting laboratory, we explored a variety environmental conditions likely account lab-to-lab variability. None these adjustments altered results. conclude example lacks robustness, confirm response, daf-7p::gfp progeny, requires sid-1 sid-2 , identify candidate siRNAs target genes mediate response.

Язык: Английский

---

Molecular Requirements for C. elegans Transgenerational Epigenetic Inheritance of Pathogen Avoidance

Опубликована: Апрель 1, 2025

C. elegans’ major food source is bacteria, and worms are naturally attracted to many bacterial species, including pathogenic Pseudomonas ; in fact, prefer PA14 as well wild bacteria over the lab E. coli strain (OP50) standardly used laboratory setting. Many labs have shown that despite this natural attraction PA14, prior exposure causes instead avoid PA14. This behavioral switch can happen on a relatively fast time scale, even within duration of choice assay. Here we show accurate assessment animals’ true first requires use paralytic (azide) trap at their initial choice, prevent from avoidance assay period. We previously discovered elegans 25°C plate-grown 20°C for 24hrs not only leads these animals switching but also progeny avoiding naïve state, persists through F4 generation. Other types training cause P0 and/or F1 avoidance, do induce transgenerational (F2 beyond) inheritance. showed (P0-F4) learned mediated by P11, small RNA produced P11 both necessary sufficient epigenetic inheritance behavior. highly expressed our standard growth conditions (25°C surfaces), other conditions, suggesting reported failure observe F2-F4 most likely due absence expression experimenters’ conditions. Through mutant analyses, tested genes – germline regulators, uptake, interference/processing, chromatin modifiers, neuronal - involvement pathogen allowing us better understand molecular requirements process. found strains TEI least two P. vranovensis fluorescens 15, avoidance. The induced each species functions specific, distinct (Pv1 Pfs1 15 , respectively) either directly or indirectly reduce levels gene maco-1 which turn regulates daf-7 ASI neuron subsequent conservation multiple components mechanism across suggests behavior be functional physiologically important

Язык: Английский

---

Behavioral adaptations of Caenorhabditis elegans against pathogenic threats

PeerJ, Год журнала: 2025, Номер 13, С. e19294 - e19294

Опубликована: Апрель 14, 2025

This review examines the behavioral adaptation mechanisms of Caenorhabditis elegans in response to pathogenic bacterial threats, emphasizing their ecological significance. It systematically explores how such as avoidance behavior, transgenerational learning, and forgetting enable C. optimize its survival reproductive strategies within dynamic microbial environments. detects harmful signals through chemosensation initiates behaviors. Simultaneously, it manages environmental energy allocation memory forgetting, allowing cope with selective pressures from fluctuations. In contrast, bacteria Pseudomonas aeruginosa Salmonella influence behavior toxin release biofilm formation, highlighting complex co-evolutionary dynamics between hosts pathogens. Additionally, these pathogens employ “Trojan Horse-like” “Worm Star” kill , further complicating host-pathogen interactions. These processes are driven by adaptations, biochemical signaling, evolutionary pressures, which emphasize niche ecosystems. serves a valuable model for studying study provides crucial theoretical insights into adaptive evolution ecosystem dynamics, offering guidance development biocontrol effective management

Язык: Английский

---

Selection on the epigenome: small RNA inheritance in animal evolution

Trends in Genetics, Год журнала: 2025, Номер unknown

Опубликована: Май 1, 2025

The inheritance of small RNAs (sRNAs) is taxonomically widespread. Changing environments alter the production and presence sRNAs in germline, this can theory either increase offspring phenotypic variance as an evolutionary bet-hedging strategy or elicit predictive adaptive responses that fitness. Nevertheless, putative role sRNA systems evolution still debated it currently unclear how selection acts on sRNAs. We outline two strategies - specialist generalist discuss non-adaptive alternatives implications different strategies. Our review suggests natural has been significantly overlooked, potentially leading to misinterpretations causal agents inheritance.

Язык: Английский

---

Molecular requirements for C. elegans transgenerational epigenetic inheritance of pathogen avoidance

eLife, Год журнала: 2025, Номер 14

Опубликована: Май 2, 2025

Bacteria are Caenorhabditis elegans’ food, and worms naturally attracted to many bacteria, including pathogenic Pseudomonas , preferring PA14 over laboratory Escherichia coli (OP50). Despite this natural attraction PA14, prior exposure causes the instead avoid PA14. This behavioral switch can happen quickly – even within duration of choice assay. We show that accurate assessment animals’ true first requires use a paralytic (azide) trap at their initial choice, preventing from avoidance assay period. previously discovered C. elegans 25°C plate-grown 20°C for 24 hr not only leads avoidance, but also four generations naïve progeny avoiding while other paradigms cause P0 and/or F1 avoidance. showed transgenerational (P0-F4) epigenetic is mediated by P11, small RNA produced P11 both necessary sufficient TEI learned highly expressed in our standard growth conditions (25°C on surfaces), conditions, suggesting reported failure observe F2-F4 likely due absence expression experimenters’ conditions. Additionally, we tested ~35 genes involvement pathogen The conservation multiple components sRNA mechanism across strains species suggests behavior be physiologically important wild

Язык: Английский

---

Coupled dopamine and insulin signaling mediated transgenerational and multigenerational inheritance of adaptive traits in Caenorhabditis elegans upon parental training with Salmonella enterica Serovar Typhi

Microbiology Spectrum, Год журнала: 2025, Номер unknown

Опубликована: Май 22, 2025

ABSTRACT The nervous system’s ability to perceive and learn about the environment can help organisms evolve acquire traits, potentially generating adaptive responses. However, its potential produce heritable modulations is a scientific lacuna, which under-explored. Here, with of Caenorhabditis elegans , has well-established neuronal networking, we found that on training worms candidate pathogenic bacterium Salmonella enterica Serovar Typhi, could exhibit characteristic transgenerational avoidance up three subsequent generations otherwise attractive pathogen. Our further analyses suggested dopamine signaling essential for learning transmission learned traits across inhibiting or mutating expression DAT-1 involved in transportation eliminated inheritance patterns. Also, offspring showed enhanced survival resistance against S . was coupled higher levels C-type lectins suggesting priming offspring’s immune system generate Typhi upon re-exposure. Enhanced DAF-2/DAF-16-mediated insulin pathway observed, inherited response be mediated through insulin/IGF-1 (IIS). Furthermore, mutigenerational continuous induced preferential adaptation better survivability toward Typhi. Taken together, present study indicates infection dopaminergic modulations, possibly key player determining decision-making host also response, by insulin-signaling pathway. IMPORTANCE Adaptation phenomenon an organism learns develops mechanism respond dynamic challenging conditions. It provides animals advantage phenotypic as well genotypic plasticity, enabling survivability. current helps understanding how environmental stresses such bacterial infections possible information experience being transmitted future generations. Neuronal promotes brain’s memory, thereby reorganizing organism. tries understand transmitting parental experiences transgenerationally. Collectively, us evolutionary adaptations exhibited generations, will long-term effects pathogenesis.

Язык: Английский

---

Pseudomonas fluorescens 15 small RNA Pfs1 mediates transgenerational epigenetic inheritance of pathogen avoidance in C. elegans through the Ephrin receptor VAB-1

bioRxiv (Cold Spring Harbor Laboratory), Год журнала: 2024, Номер unknown

Опубликована: Май 23, 2024

Abstract C. elegans are exposed to a variety of pathogenic and non-pathogenic bacteria species in their natural environment. Correspondingly, has evolved an ability discern between nutritive infectious bacterial food sources. Here we show that can learn avoid the Pseudomonas fluorescens 15 (PF15), this learned avoidance behavior is passed on progeny for four generations, as previously demonstrated aeruginosa (PA14) vranovensis , using similar mechanisms, including involvement both TGF-β ligand DAF-7 Cer1 retrotransposon-encoded virus-like particles. PF15 small RNAs necessary sufficient induce transgenerational behavior. Unlike PA14 or P. does not use P11, Pv1, RNA with maco-1 homology avoidance; instead, unrelated RNA, Pfs1, targets vab-1 Ephrin receptor gene avoidance, suggesting evolution yet another sRNA/ target pair involved inheritance pathogen avoidance. As VAB-2 MACO-1 knockdown also have begun understand genetic pathway targeted Moreover, these data axon guidance genes (VAB-1 VAB-2) unknown adult roles regulating neuronal function. may multiple specificity-encoded RNA-dependent mechanisms different species, thereby providing survival advantage dynamic

Язык: Английский

---

Reported transgenerational responses to Pseudomonas aeruginosa in C. elegans are not robust

eLife, Год журнала: 2024, Номер unknown

Опубликована: Авг. 21, 2024

Here we report our attempt to replicate reports of transgenerational epigenetic inheritance in Caenorhabditis elegans . Published results from multiple laboratories show that C. adults and their F1 embryos exposed the pathogen Pseudomonas aeruginosa aversion behavior a exposure-dependent increase daf-7/TGFβ reporter gene expression. However, one group persistence elevated daf-7 expression F2, F3, F4 generations. In contrast, failed consistently detect either avoidance response or beyond generation. We did confirm dsRNA transport proteins SID-1 SID-2 are required for intergenerational (F1) avoidance, but not Furthermore, reanalysis RNA seq data provides additional evidence this inherited PA14 may be mediated by small RNAs. The experimental methods well-described, source materials readily available, including samples reporting laboratory, explored variety environmental conditions likely account lab-to-lab variability. None these adjustments altered results. conclude example lacks robustness, response, daf-7p::gfp progeny, requires sid-1 sid-2 , identify candidate siRNAs target genes mediate response.

Язык: Английский

---