Parasitic Nematodes Exert Antimicrobial Activity and Benefit From Microbiota-Driven Support for Host Immune Regulation

Rausch, Sebastian; Midha, Ankur; Kuhring, Mathias; Affinass, Nicole; Radonić, Aleksandar; Kühl, Anja A.; Bleich, André; Renard, Bernhard Y.; Hartmann, Susanne

doi:10.3389/fimmu.2018.02282

Cited by 70 publications

(89 citation statements)

References 78 publications

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“…Our observation that axenic helminth infection results in impaired parasite fecundity is consistent with previous reports 16,17 . In addition to this reduction in fitness, we observed a non-significant, but trending decrease in worm burden in germ-free mice infected with Hpb HA107 at two weeks postinfection.…”

Section: Discussionsupporting

confidence: 94%

“…Our description of a detailed methodology for rearing effectively germ-free Hpb larvae expands on previous work 5 and validates this model for in vivo studies. This technique will serve as an alternative to other methods of sterilizing Hpb such as antibiotic treatment of the L3 larvae prior to infection of germ-free mice 16 . Our methodology provides two improvements over such approaches.…”

Section: Discussionmentioning

confidence: 99%

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The gut microbiota limits Th2 immunity toHeligmosomoides polygyrus bakeriinfection

Russell

Faubert

Verdú

et al. 2020

Preprint

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Helminth-induced alterations to the gut microbiota have been shown to affect immune responses at local and peripheral sites. Studies examining helminth-microbiota interactions, however, have been limited due to the practical constraints of performing germ-free experiments with parasites that thrive in microbial-rich conditions to complete their development. The infectious (L3) larvae of the murine helminth Heligmosomoides polygyrus bakeri (Hpb), for example, are normally reared using a fecal-culture method and therefore are inherently unsuitable for germ-free studies in vivo. Herein, we detail an adapted methodology for rearing effectively germ-free Hpb larvae that are able to maintain the axenic status of a germ-free host during infection. We validate that these larvae do not display any fitness defects relative to fecal-grown larvae and evoke a comparable immune response in vivo. Characterization of axenic Hpb infection reveals that the commensal microbiota play a multifaceted role during infection -curbing the anti-Hpb Th2 response and directing the resolution of tissue granulomas, while simultaneously promoting parasite fitness. Overall these data demonstrate a mutualistic relationship between commensal microbes, enteric helminths and the infected host.

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Section: Discussionsupporting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

The gut microbiota limits Th2 immunity toHeligmosomoides polygyrus bakeriinfection

Russell

Faubert

Verdú

et al. 2020

Preprint

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“…However, reports indicate that sea lice and salmon mucus microbiota are not necessarily correlated 19 , and this supports the findings of this study where a stable, robust core microbiome was identified regardless region, center, producer practices or other factor. The factors influencing the stability of the core community are yet to be unraveled, but it is known that other parasites such as the nematode Heligmosomoides polygyrus can secrete antimicrobial compounds that shape the host-microbiota for the parasite's benefit, increasing its fitness 39 . It is known that sea lice developed a complex secretome 40 , that modulates host immune response 41 , and host mucus microbiome 19 .…”

Section: Discussionmentioning

confidence: 99%

Nanopore sequencing of microbial communities reveals the potential role of sea lice as a reservoir for fish pathogens

Gonçalves

Collipal-Matamal

Valenzuela-Muñoz

et al. 2020

Sci Rep

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Caligus rogercresseyi is a copepod ectoparasite with a high prevalence in salmon farms in Chile, causing severe welfare and economic concerns to the sector. information on the parasite's underpinning mechanisms to support its life strategy is recently being investigated. Due to the critical role of microbiota, this study aimed to characterize the microbiota community associated with C. rogercresseyi from different regions with salmon aquaculture in Chile. Using third-generation sequencing with Nanopore technology (MinION) the full 16S rRNA gene from sea lice obtained from 8 areas distributed over the three main aquaculture regions were sequenced. Microbiota of the parasite is mainly comprised of members of phyla Proteobacteria and Bacteroidetes, and a core microbiota community with 147 taxonomical features was identified, and it was present in sea lice from the three regions. This community accounted for 19% of total identified taxa but more than 70% of the total taxonomical abundance, indicating a strong presence in the parasite. Several taxa with bioactive compound secretory capacity were identified, such as members of genus Pseudoalteromonas and Dokdonia, suggesting a possible role of the lice microbiota during the host infestation processes. Furthermore, the microbiota community was differentially associated with the salmon production, where several potential pathogens such as Vibrio, Tenacibaculum, and Aeromonas in Los Lagos, Aysén, and Magallanes region were identified. Notably, the Chilean salmon industry was initially established in the Los Lagos region but it's currently moving to the south, where different oceanographic conditions coexist with lice populations. The results originated by this study will serve as foundation to investigate putative role of sea lice as vectors for fish pathogens and also as reservoirs for antibiotic-resistant genes.The copepod Caligus rogercresseyi, a caligid ectoparasite that is commonly found in southern Chilean salmon farms, is one of most impacting sanitary issues of the industry 1,2 . C. rogercresseyi infestation has a profound effect on fish, producing irritation, loss of scales and skin wounds that may lead to secondary infections, producing strong physiological 3,4 and molecular responses 2,5 in the host. These contribute to a decrease in fish health causing an estimated production cost of 1.4USD per kilogram of produced salmon 6 . Despite the different types of available treatments, bath and oral application of delousing drugs are still preferred 7 . However, reduced sensitivity compromising treatment efficiency for organophosphates and pyrethroids have been recently reported in Chile 8 . The usage of advanced molecular biology tools such as high-throughput sequencing allowed a substantial increase of information regarding the parasite's invasive and defensive strategies within the parasite-host interface, and during exposure to delousing drugs over the past years (reviewed by et al. 2 ). Despite that, to date there is no available information regarding C. rogerc...

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“…Another mechanism that helminths could use to alter the microbiota is the secretion of excretory/secretory (ES) products, which have mainly been studied in the context of immunomodulation . Recent evidence showed that these products could have a direct inhibitory effect on bacteria growth (Figure ) . Whilst most data demonstrating the ability of helminths to alter the intestinal microbiota have been acquired through studies in rodents, evidence in humans also exists indicating this is likely to occur across multiple parasitic and host species …”

Section: Helminth Infection and Metabolic Statusmentioning

confidence: 99%

“…78 Recent evidence showed that these products could have a direct inhibitory effect on bacteria growth (Figure 2). 79 Whilst most data demonstrating the ability of helminths to alter the intestinal microbiota have been acquired through studies in rodents, evidence in humans also exists indicating this is likely to occur across multiple parasitic and host species. [80][81][82] Helminth-induced alterations to microbial communities have important functional consequences for the host as demonstrated in a recent study from our own group that showed that H. polygyrus infection provides protection against asthma by modulating the intestinal microbiota to increase the availability of short-chain fatty acids (SCFA).…”

Section: Possible Contribution Of Helminthmicrobiota Interactions On mentioning

confidence: 99%

The interplay of type 2 immunity, helminth infection and the microbiota in regulating metabolism

2019

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Type 2 immunity has recently emerged as a critical player in metabolic status, with numerous studies investigating the role of type 2 immune cells within adipose tissue. Metabolic dysfunction is often characterised as a low‐grade or chronic inflammatory state within tissues, and type 2 immunity may facilitate a return to metabolic homeostasis. A complex network of type 2 resident cells including M2 macrophages, eosinophils and ILC2s has been identified within adipose tissue. Although the effector cells in this equilibrium have not been clearly identified, any alteration of the type 2 microenvironment resulted in an altered metabolic state. Historically, the type 2 immune response has been associated with helminth infection. The type 2 immune response drives host resistance and plays an important role in promoting tissue repair following the migration of helminth larvae through tissues. Although helminths are largely eradicated in developed countries, infection rates remain high in poor communities within the developing world. Interestingly, there is strong evidence that helminth infection is inversely correlated with autoimmune or inflammatory disorders. Recently, an increasing amount of epidemiological and field studies suggest that it could be the same for obesity and metabolic syndrome. In the current review, we summarise the literature linking type 2 immunity to improved adipose tissue function. We then discuss more recent evidence indicating that helminth infection can provide protection against metabolic syndrome. Lastly, we explore the possible contributions of altered nutrient uptake, adipose tissue function and/or the intestinal microbiota with the ability of helminths to alter metabolic status.

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Parasitic Nematodes Exert Antimicrobial Activity and Benefit From Microbiota-Driven Support for Host Immune Regulation

Cited by 70 publications

References 78 publications

The gut microbiota limits Th2 immunity toHeligmosomoides polygyrus bakeriinfection

The gut microbiota limits Th2 immunity toHeligmosomoides polygyrus bakeriinfection

Nanopore sequencing of microbial communities reveals the potential role of sea lice as a reservoir for fish pathogens

The interplay of type 2 immunity, helminth infection and the microbiota in regulating metabolism

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