scholarly journals Vertical transmission of tissue microbiota in Caenorhabditis elegans

2021 ◽  
Author(s):  
Jun Zheng ◽  
Xin Meng ◽  
Jiahao Fan ◽  
Dong Yang

AbstractThe past forty-five years has witnessed Caenorhabditis elegans as the most significant model animal in life science since its discovery seventy years ago1,2, as it introduced principles of gene regulated organ development, and RNA interference into biology3-5. Meanwhile, it has become one of the lab animals in gut microbiota studies as these symbionts contribute significantly to many aspects in host biology6,7. Meanwhile, the origin of gut microbiota remains debatable in human8- 11, and has not been investigated in other model animals. Here we show that the symbiont bacteria in C. elegans not only vertically transmit from the parent generation to the next, but also distributes in the worm tissues parallel with its development. We found that bacteria can enter into the embryos of C. elegans, a step associated with vitellogenin, and passed to the next generation. These vertically transmitted bacteria share global similarity, and bacterial distribution in worm tissues changes as they grow at different life stages. Antibiotic treatment of worms increased their vulnerability against pathogenic bacteria, and replenishment of tissue microbiota restored their immunity. These results not only offered a molecular basis of vertical transmission of bacteria in C. elegans, but also signal a new era for the mixed tissue cell-bacteria multi-species organism study.

Nutrients ◽  
2018 ◽  
Vol 10 (12) ◽  
pp. 1921 ◽  
Author(s):  
Maiko Kato ◽  
Yumi Hamazaki ◽  
Simo Sun ◽  
Yoshikazu Nishikawa ◽  
Eriko Kage-Nakadai

Clostridium butyricum MIYAIRI 588 (CBM 588), one of the probiotic bacterial strains used for humans and domestic animals, has been reported to exert a variety of beneficial health effects. The effect of this probiotic on lifespan, however, is unknown. In the present study, we investigated the effect of CBM 588 on lifespan and multiple-stress resistance using Caenorhabditis elegans as a model animal. When adult C. elegans were fed a standard diet of Escherichia coli OP50 or CBM 588, the lifespan of the animals fed CBM 588 was significantly longer than that of animals fed OP50. In addition, the animals fed CBM588 exhibited higher locomotion at every age tested. Moreover, the worms fed CBM 588 were more resistant to certain stressors, including infections with pathogenic bacteria, UV irradiation, and the metal stressor Cu2+. CBM 588 failed to extend the lifespan of the daf-2/insulin-like receptor, daf-16/FOXO and skn-1/Nrf2 mutants. In conclusion, CBM 588 extends the lifespan of C. elegans probably through regulation of the insulin/IGF-1 signaling (IIS) pathway and the Nrf2 transcription factor, and CBM 588 improves resistance to several stressors in C. elegans.


2019 ◽  
Vol 17 (2) ◽  
pp. 150-162
Author(s):  
Priya Patel ◽  
Hiteshi Patel ◽  
Dhara Vekariya ◽  
Chinmayi Joshi ◽  
Pooja Patel ◽  
...  

<P>Background: In view of the global threat of antimicrobial resistance, novel alternative approaches to deal with infectious bacteria are warranted, in addition to the conventional invasive therapeutic approaches. Objective: This study aimed at investigating whether exposure to sonic stimulation or microwave radiation can affect virulence of pathogenic bacteria toward the model nematode host Caenorhabditis elegans. Methods: Caenorhabditis elegans worms infected with different pathogenic bacteria were subjected to sonic treatment to investigate whether such sound treatment can exert any therapeutic effect on the infected worms. Virulence of microwave exposed bacteria was also assessed using this nematode host. Results: Sound corresponding to 400 Hz, and the divine sound ‘Om’ conferred protective effect on C. elegans in face of bacterial infection, particularly that caused by Serratia marcescens or Staphylococcus aureus. The observed effect seemed to occur due to influence of sound on bacteria, and not on the worm. Additionally, effect of microwave exposure on bacterial virulence was also investigated, wherein microwave exposure could reduce virulence of S. aureus towards C. elegans. Conclusion: Sonic stimulation/ microwave exposure was demonstrated to be capable of modulating bacterial virulence.</P>


mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Carolaing Gabaldón ◽  
Marcela Legüe ◽  
M. Fernanda Palominos ◽  
Lidia Verdugo ◽  
Florence Gutzwiller ◽  
...  

ABSTRACT The interaction and communication between bacteria and their hosts modulate many aspects of animal physiology and behavior. Dauer entry as a response to chronic exposure to pathogenic bacteria in Caenorhabditis elegans is an example of a dramatic survival response. This response is dependent on the RNA interference (RNAi) machinery, suggesting the involvement of small RNAs (sRNAs) as effectors. Interestingly, dauer formation occurs after two generations of interaction with two unrelated moderately pathogenic bacteria. Therefore, we sought to discover the identity of C. elegans RNAs involved in pathogen-induced diapause. Using transcriptomics and differential expression analysis of coding and long and small noncoding RNAs, we found that mir-243-3p (the mature form of mir-243) is the only transcript continuously upregulated in animals exposed to both Pseudomonas aeruginosa and Salmonella enterica for two generations. Phenotypic analysis of mutants showed that mir-243 is required for dauer formation under pathogenesis but not under starvation. Moreover, DAF-16, a master regulator of defensive responses in the animal and required for dauer formation was found to be necessary for mir-243 expression. This work highlights the role of a small noncoding RNA in the intergenerational defensive response against pathogenic bacteria and interkingdom communication. IMPORTANCE Persistent infection of the bacterivore nematode C. elegans with bacteria such as P. aeruginosa and S. enterica makes the worm diapause or hibernate. By doing this, the worm closes its mouth, avoiding infection. This response takes two generations to be implemented. In this work, we looked for genes expressed upon infection that could mediate the worm diapause triggered by pathogens. We identify mir-243-3p as the only transcript commonly upregulated when animals feed on P. aeruginosa and S. enterica for two consecutive generations. Moreover, we demonstrate that mir-243-3p is required for pathogen-induced dauer formation, a new function that has not been previously described for this microRNA (miRNA). We also find that the transcriptional activators DAF-16, PQM-1, and CRH-2 are necessary for the expression of mir-243 under pathogenesis. Here we establish a relationship between a small RNA and a developmental change that ensures the survival of a percentage of the progeny.


2015 ◽  
Vol 84 (2) ◽  
pp. 524-536 ◽  
Author(s):  
Corin V. White ◽  
Brian J. Darby ◽  
Robert J. Breeden ◽  
Michael A. Herman

Stenotrophomonas maltophiliais a ubiquitous bacterium and an emerging nosocomial pathogen. This bacterium is resistant to many antibiotics, associated with a number of infections, and a significant health risk, especially for immunocompromised patients. Given thatCaenorhabditis elegansshares many conserved genetic pathways and pathway components with higher organisms, the study of its interaction with bacterial pathogens has biomedical implications.S. maltophiliahas been isolated in association with nematodes from grassland soils, and it is likely thatC. elegansencounters this bacterium in nature. We found that a localS. maltophiliaisolate, JCMS, is more virulent than the otherS. maltophiliaisolates (R551-3 and K279a) tested. JCMS virulence correlates with intestinal distension and bacterial accumulation and requires the bacteria to be alive. Many of the conserved innate immune pathways that serve to protectC. elegansfrom various pathogenic bacteria also play a role in combatingS. maltophiliaJCMS. However,S. maltophiliaJCMS is virulent to normally pathogen-resistant DAF-2/16 insulin-like signaling pathway mutants. Furthermore, several insulin-like signaling effector genes were not significantly differentially expressed betweenS. maltophiliaJCMS and avirulent bacteria (Escherichia coliOP50). Taken together, these findings suggest thatS. maltophiliaJCMS evades the pathogen resistance conferred by the loss of DAF-2/16 pathway components. In summary, we have discovered a novel host-pathogen interaction betweenC. elegansandS. maltophiliaand established a new animal model with which to study the mode of action of this emerging nosocomial pathogen.


2017 ◽  
Vol 23 (8) ◽  
pp. 656-666 ◽  
Author(s):  
Yi Xiao ◽  
Fang Liu ◽  
Pei-ji Zhao ◽  
Cheng-Gang Zou ◽  
Ke-Qin Zhang

The genetically tractable organism Caenorhabditis elegans is a powerful model animal for the study of host innate immunity. Although the intestine and the epidermis of C. elegans that is in contact with pathogens are likely to function as sites for the immune function, recent studies indicate that the nervous system could control innate immunity in C. elegans. In this report, we demonstrated that protein kinase A (PKA)/KIN-1 in the neurons contributes to resistance against Salmonella enterica infection in C. elegans. Microarray analysis revealed that PKA/KIN-1 regulates the expression of a set of antimicrobial effectors in the non-neuron tissues, which are required for innate immune responses to S. enterica. Furthermore, PKA/KIN-1 regulated the expression of lysosomal genes during S. enterica infection. Our results suggest that the lysosomal signaling molecules are involved in autophagy by controlling autophagic flux, rather than formation of autophagosomes. As autophagy is crucial for host defense against S. enterica infection in a metazoan, the lysosomal pathway also acts as a downstream effector of the PKA/KIN-1 signaling for innate immunity. Our data indicate that the PKA pathway contributes to innate immunity in C. elegans by signaling from the nervous system to periphery tissues to protect the host against pathogens.


mBio ◽  
2017 ◽  
Vol 8 (5) ◽  
Author(s):  
M. Fernanda Palominos ◽  
Lidia Verdugo ◽  
Carolaing Gabaldon ◽  
Bernardo Pollak ◽  
Javiera Ortíz-Severín ◽  
...  

ABSTRACT The dynamic response of organisms exposed to environmental pathogens determines their survival or demise, and the outcome of this interaction depends on the host’s susceptibility and pathogen-dependent virulence factors. The transmission of acquired information about the nature of a pathogen to progeny may ensure effective defensive strategies for the progeny’s survival in adverse environments. Environmental RNA interference (RNAi) is a systemic and heritable mechanism and has recently been linked to antibacterial and antifungal defenses in both plants and animals. Here, we report that the second generation of Caenorhabditis elegans living on pathogenic bacteria can avoid bacterial infection by entering diapause in an RNAi pathway-dependent mechanism. Furthermore, we demonstrate that the information encoding this survival strategy is transgenerationally transmitted to the progeny via the maternal germ line. IMPORTANCE Bacteria vastly influence physiology and behavior, and yet, the specific mechanisms by which they cause behavioral changes in hosts are not known. We use C. elegans as a host and the bacteria they eat to understand how microbes trigger a behavioral change that helps animals to survive. We found that animals faced with an infection for two generations could enter a hibernationlike state, arresting development by forming dauer larvae. Dauers have closed mouths and effectively avoid infection. Animals accumulate information that is transgenerationally transmitted to the next generations to form dauers. This work gives insight on how bacteria communicate in noncanonical ways with their hosts, resulting in long-lasting effects providing survival strategies to the community. IMPORTANCE Bacteria vastly influence physiology and behavior, and yet, the specific mechanisms by which they cause behavioral changes in hosts are not known. We use C. elegans as a host and the bacteria they eat to understand how microbes trigger a behavioral change that helps animals to survive. We found that animals faced with an infection for two generations could enter a hibernationlike state, arresting development by forming dauer larvae. Dauers have closed mouths and effectively avoid infection. Animals accumulate information that is transgenerationally transmitted to the next generations to form dauers. This work gives insight on how bacteria communicate in noncanonical ways with their hosts, resulting in long-lasting effects providing survival strategies to the community.


2012 ◽  
Vol 58 (11) ◽  
pp. 1268-1277 ◽  
Author(s):  
Arihiro Osanai ◽  
Dong-Liang Hu ◽  
Akio Nakane

Avoidance behavior of Caenorhabditis elegans, a nematode, towards Staphylococcus aureus, a pathogenic bacterium, was studied. Caenorhabditis elegans avoided S. aureus cultures and also their culture supernatants, suggesting that secretory molecules are involved in the repellent activity. We demonstrated that toxic shock syndrome toxin 1 (TSST-1) and staphylococcal enterotoxin C (SEC), the superantigenic toxins produced by S. aureus, are responsible for the nematode avoidance. By using TSST-1 and SEC mutants, the results indicated that the repellent activity of these toxins is independent of their superantigenic activity. The TSST-1 and SEC were found to locate at chemosensory neurons that are responsible for the recognition of repellents and avoidance of pathogenic bacteria. When mutants of C. elegans deficient in Toll/interleukin-1 receptor (TIR-1) and 5-hydroxytryptamine (5-HT) biosynthesis were used, avoidance behavior was attenuated. In the 5-HT biosynthesis deficient mutant nematodes, the avoidance activity was recovered when exogenous 5-HT was added. tph-1 expression and 5-HT production were upregulated when the nematodes were treated with TSST-1 or SEC. These results suggest that C. elegans avoids S. aureus by recognizing secretory molecules including TSST-1 and SEC and this avoidance is dependent on TIR and production of 5-HT.


2003 ◽  
Vol 66 (11) ◽  
pp. 1964-1971 ◽  
Author(s):  
KRISHAUN N. CALDWELL ◽  
GARY L. ANDERSON ◽  
PHILLIP L. WILLIAMS ◽  
LARRY R. BEUCHAT

Caenorhabditis elegans was studied to determine the potential role of free-living microbivorous nematodes as vectors for preharvest contamination of fruits and vegetables with foodborne pathogens. The propensity of C. elegans to be attracted to seven strains of Escherichia coli O157:H7, eight serotypes of Salmonella, six strains of Listeria monocytogenes, and cantaloupe juice was investigated. Twenty to 30 adult worms were placed on the surface of K agar midway between a 24-h bacterial colony and 10 μl of uninoculated tryptic soy broth (TSB) or cantaloupe juice positioned 1.5 cm apart. The numbers of nematodes that migrated to the colony, to the TSB, and to the cantaloupe juice within 5, 10, 15, and 20 min at 21°C were determined, and then the plates were incubated at 37°C for up to 7 days to determine the ability of C. elegans to survive and reproduce in bacterial colonies. The nematode was attracted to colonies of all test pathogens and survived and reproduced within colonies for up to 7 days. C. elegans was not attracted to cantaloupe juice. The potential of C. elegans to serve as a vector for the transport of Salmonella Poona to cantaloupe rinds was investigated. Adult worms that had been immersed in a suspension of Salmonella Poona were deposited 1 or 3 cm below the surface of soil on which a piece of cantaloupe rind was placed. The rind was analyzed for the presence of Salmonella Poona after 1, 3, 7, and 10 days at 21°C. The presence of Salmonella Poona was evident more quickly on rinds positioned on soil beneath which C. elegans inoculated with Salmonella Poona was initially deposited than on rinds positioned on soil beneath which Salmonella Poona alone was deposited. The time required to detect Salmonella Poona on rinds was longer when the rind was placed 3 cm above the inoculum than when the rind was placed 1 cm above the inoculum. Free-living nematodes may play a role in the preharvest dispersal of incidental human pathogens in soil to the surfaces of raw fruits and vegetables in contact with soil during development and maturation, as evidenced by the behavior of C. elegans as a test model.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Miroslav Dinić ◽  
Stefan Jakovljević ◽  
Jelena Đokić ◽  
Nikola Popović ◽  
Dušan Radojević ◽  
...  

AbstractThe host-microbiota cross-talk represents an important factor contributing to innate immune response and host resistance during infection. It has been shown that probiotic lactobacilli exhibit the ability to modulate innate immunity and enhance pathogen elimination. Here we showed that heat-inactivated probiotic strain Lactobacillus curvatus BGMK2-41 stimulates immune response and resistance of the Caenorhabditis elegans against Staphylococcus aureus and Pseudomonas aeruginosa. By employing qRT-PCR and western blot analysis we showed that heat-inactivated BGMK2-41 activated PMK-1/p38 MAPK immunity pathway which prolongs the survival of C. elegans exposed to pathogenic bacteria in nematode killing assays. The C. elegans pmk-1 mutant was used to demonstrate a mechanistic basis for the antimicrobial potential of BGMK2-41, showing that BGMK2-41 upregulated PMK-1/p38 MAPK dependent transcription of C-type lectins, lysozymes and tight junction protein CLC-1. Overall, this study suggests that PMK-1/p38 MAPK‐dependent immune regulation by BGMK2-41 is essential for probiotic-mediated C. elegans protection against gram-positive and gram-negative bacteria and could be further explored for development of probiotics with the potential to increase resistance of the host towards pathogens.


2021 ◽  
Author(s):  
Patrick Lansdon ◽  
Maci Carlson ◽  
Brian D Ackley

The soil-dwelling nematode Caenorhabditis elegans serves as a model system to study innate immunity against microbial pathogens. C. elegans have been collected from around the world, where they, presumably, adapted to regional microbial ecologies. Here we use survival assays and RNA-sequencing to better understand how two isolates from disparate climates respond to pathogenic bacteria. We found that, relative to N2 (originally isolated in Bristol, UK), CB4856 (isolated in Hawaii), was more susceptible to the Gram-positive pathogen, Staphylococcus epidermidis, but equally susceptible to Staphylococcus aureus as well as two Gram-negative pathogens, Providencia rettgeri and Pseudomonas aeruginosa. We performed transcriptome analysis of infected worms and found gene-expression profiles were considerably different in an isolate-specific and pathogen-specific manner. We performed GO term analysis to categorize differential gene expression in response to S. epidermidis. In N2, genes that encoded detoxification enzymes and extracellular matrix proteins were significantly enriched, while in CB4856, genes that encoded detoxification enzymes, C-type lectins, and lipid metabolism proteins were enriched, suggesting they have different responses to these bacterial pathogens, despite being the same species. Overall, discerning gene expression signatures in an isolate by pathogen manner can help us to understand the different possibilities for the evolution of immune responses within organisms.


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