Parental dietary vitamin B12 causes intergenerational growth acceleration and protects offspring from pathogenic microsporidia and bacteria.

The parental environment of C. elegans can have lasting effects on progeny development and immunity. Vitamin B12 exposure in C. elegans has been shown to accelerate development and protect against pathogenic bacteria. Here, we show that parental exposure to dietary vitamin B12 or vitamin B12-producing bacteria results in offspring with accelerated growth that persists for a single generation. During infection with the microsporidian Nematocida parisii, the offspring of worms fed vitamin B12 diets have better reproductive fitness but similar infection levels, suggesting increased tolerance to microsporidian infection. Vitamin B12-induced intergenerational growth acceleration and N. parisii tolerance is dependent upon the methionine biosynthesis pathway. Offspring from vitamin B12-exposed parents are protected from pathogenic Pseudomonas vranovensis and this protection is mediated through methionine biosynthesis and propionyl-CoA breakdown pathways. Our results show how parental microbial diet impacts progeny development through the transfer of vitamin B12 which results in accelerated growth and pathogen tolerance.

Generation of a Microsporidia Species Attribute Database and Analysis of the Extensive Ecological and Phenotypic Diversity of Microsporidia.

Microsporidia are a large group of fungus-related obligate intracellular parasites. Though many microsporidia species have been identified over the past 160 years, depiction of the full diversity of this phylum is lacking. To systematically describe the characteristics of these parasites, we created a database of 1,440 species and their attributes, including the hosts they infect and spore characteristics. We find that microsporidia have been reported to infect 16 metazoan and 4 protozoan phyla, with smaller phyla being underrepresented. Most species are reported to infect only a single host, but those that are generalists are also more likely to infect a broader set of host tissues. Strikingly, polar tubes are threefold longer in species that infect tissues besides the intestine, suggesting that polar tube length is a determinant of tissue specificity. Phylogenetic analysis revealed four clades which each contain microsporidia that infect hosts from all major habitats. Although related species are more likely to infect similar hosts, we observe examples of changes in host specificity and convergent evolution. Taken together, our results show that microsporidia display vast diversity in their morphology and the hosts they infect, illustrating the flexibility of these parasites to evolve new traits. IMPORTANCE Microsporidia are a large group of parasites that cause death and disease in humans and many agriculturally important animal species. To fully understand the diverse properties of these parasites, we curated species reports from the last 160 years. Using these data, we describe when and where microsporidia were identified and what types of animals and host tissues these parasites infect. Microsporidia infect hosts using a conserved apparatus known as the polar tube. We observe that the length of this tube is correlated with the tissues that are being infected, suggesting that the polar tube controls where within the animals that the parasite infects. Finally, we show that microsporidia species often exist in multiple environments and are flexible in their ability to evolve new traits. Our study provides insight into the ecology and evolution of microsporidia and provides a useful resource to further understand these fascinating parasites.

A parental transcriptional response to microsporidia infection induces inherited immunity in offspring.

Parental infection can result in the production of offspring with enhanced immunity phenotypes. Critically, the mechanisms underlying inherited immunity are poorly understood. Here, we show that Caenorhabditis elegans infected with the intracellular microsporidian parasite N. parisii produce progeny that are resistant to microsporidia infection. We determine the kinetics of the response and show that intergenerational immunity prevents host-cell invasion by Nematocida parisii and enhances survival to the bacterial pathogen Pseudomonas aeruginosa We demonstrate that immunity is induced by the parental transcriptional response to infection, which can be mimicked through maternal somatic depletion of PALS-22 and the retinoblastoma protein ortholog, LIN-35. We find that other biotic and abiotic stresses (viral infection and cadmium exposure) that induce a similar transcriptional response as microsporidia also induce immunity in progeny. Together, our results reveal how a parental transcriptional signal can be induced by distinct stimuli and protect offspring against multiple classes of pathogens.

Remembering your enemies: mechanisms of within-generation and multigenerational immune priming in Caenorhabditis elegans.

Pathogens are abundant and drive evolution of host immunity. Whilst immune memory is classically associated with adaptive immunity, studies in diverse species now show that priming of innate immune defences can also protect against secondary infection. Remarkably, priming may also be passed on to progeny to enhance pathogen resistance and promote survival in future generations. Phenotypic changes that occur independent of DNA sequence underlie both 'within-generation' priming and 'multigenerational' priming. However, the molecular mechanisms responsible for these phenomena are still poorly understood. Caenorhabditis elegans is a simple and genetically tractable model organism that has enabled key advances in immunity and environmental epigenetics. Using both natural and human pathogens, researchers have uncovered numerous examples of innate immune priming in this animal. Viral infection models have provided key evidence for a conserved antiviral RNA silencing mechanism that is inherited in progeny. Bacterial infection models have explored mechanisms of within-generation and multigenerational priming that span chromatin modification and transcriptional changes, small RNA pathways, maternal provisioning and pathogen avoidance strategies. Together, these studies are providing novel insight into the immune reactivity of the genome and have important consequences for our understanding of health and evolution. In this review, we present the current evidence for learned protection against pathogens in C. elegans, discuss the significance and limitations of these findings and highlight important avenues of future investigation.