Helminth-microbiota cross-talk – A journey through the vertebrate digestive system

Abstract

The gastrointestinal (GI) tract of vertebrates is inhabited by a vast array of organisms, that is, the microbiota and macrobiota. The former is composed largely of commensal microorganisms, which play vital roles in host nutrition and maintenance of energy balance, in addition to supporting the development and function of the vertebrate immune system. By contrast, the macrobiota includes parasitic helminths, which are mostly considered detrimental to host health via a range of pathogenic effects that depend on parasite size, location in the GI tract, burden of infection, metabolic activity, and interactions with the host immune system. Sharing the same environment within the vertebrate host, the GI microbiota and parasitic helminths interact with each other, and the results of such interactions may impact, directly or indirectly, on host health and homeostasis. The complex relationships occurring between parasitic helminths and microbiota have long been neglected; however, recent studies point towards a role for these interactions in the overall pathophysiology of helminth disease, as well as in parasite-mediated suppression of inflammation. Whilst several discrepancies in qualitative and quantitative modifications in gut microbiota composition have been described based on host and helminth species under investigation, we argue that attention should be paid to the systems biology of the gut compartment under consideration, as variations in the abundances of the same population of bacteria inhabiting different niches of the GI tract may result in varying functional consequences for host physiology.

Fasciola hepatica-Derived Molecules as Regulators of the Host Immune Response

“…Furthermore, as helminths have a multistage life cycle with distinct developmental stages through select tissues and organ systems, they may release distinct molecules within a particular niche (e.g., the intestine or lung) or migratory stages that exert more localized immunomodulatory effects ( 94 ), which may be of relevance for targeting tissue-specific inflammation. As recently reviewed by Cortés et al ( 95 ) and van der Zande et al ( 9 ), a number of studies have identified potential roles for helminth-host microbiome interaction in the pathophysiology of helminth disease and in parasite-mediated suppression of host inflammation, which may be relevant for the targeting of gut and lung inflammation and (immuno)metabolic dysfunction. In addition to the protein molecules outlined herein, there are a number of other families of helminth immunomodulators, which include various carbohydrate, nucleotide and lipid mediators as well as extracellular vesicles that require further investigation ( 16 ).…”

2-Methyl-pentanoyl-carnitine (2-MPC): a urine biomarker for patent Ascaris lumbricoides infection

“…Although the data presented here suggest a direct connection between the presence of A. lumbricoides and 2-MPC in urine, it cannot be excluded that 2-methyl valeric acid (and consequently, its carnitine ester 2-MPC) is in fact produced by gut bacteria. There are several reports that indicate intestinal parasites, such as A. lumbricoides, increase host gut microbiome diversity [29][30][31][32][33] . This interplay between host, microbiome and macrobiome might lead to an altered production of certain short-chain fatty acids (SCFAs) by the microbiome.…”

The immune response and microbiota profiles during co-infection with P. vivax and soil-transmitted helminths

“…Nonetheless, every study population has unique characteristics, and in other study sites, such trends have not been observed Cooper et al 2013). Large-intestinal-dwelling helminths, such as Trichuris trichiura, may have different effects on the microbiota than small-intestinal and tissue-dwelling helminths (Cortés et al 2019). Additionally, the effects of the anti-helminthic drugs on the microbiota is still not definitively understood.…”

“…The effects of helminths on the gut microbiota have also been increasingly documented (Cortés et al 2019). By characterizing the microbiota of a group of indigenous Malaysians known as the Orang Asli using 16S rRNA gene sequencing, we previously found that STH-infected individuals have greater microbial diversity than uninfected individuals (Lee et al 2014).…”