Trends in Parasitology

Trends in Parasitology

Volume 35, Issue 1, January 2019, Pages 13-22
Journal home page for Trends in Parasitology

Opinion
Helminth Microbiomes – A Hidden Treasure Trove?

https://doi.org/10.1016/j.pt.2018.10.007Get rights and content

Highlights

In spite of a plethora of evidence supporting key roles of resident bacteria for parasite fitness and survival (i.e., in filarial nematodes and whipworms), little is known of microbial populations inhabiting organs and tissues of gastrointestinal nematodes of major socioeconomic significance.

To date, one of the few well characterised examples is the symbiotic relationship between bacteria of the genus Wolbachia and filarial nematodes.

Notably, our understanding of this symbiosis has already been successfully exploited for therapeutic purposes.

The relentless advancement in sequencing techniques, together with the rise of novel microbiome editing tools provide unprecedented opportunities to investigate helminth microbiomes and exploit parasite–microbiome relationships for the development of novel strategies of parasite control.

There is increasing attention on the complex interactions occurring between gastrointestinal parasitic helminths and the microbial flora (microbiota) inhabiting the host gut. However, little is known about the occurrence, structure, and function of microbial populations residing within parasite organs and tissues. In this article, we argue that an in-depth understanding of the interplay between parasites and their microbiomes may significantly enhance current knowledge of parasite biology and physiology, and may lead to the discovery of entirely novel, anthelmintic-independent interventions against parasites and parasitic diseases.

Section snippets

Gastrointestinal Helminths – Worm Guts within Host Guts

The gastrointestinal (GI) tract of vertebrates is inhabited by 10–100 trillion microorganisms, including bacteria, viruses, fungi, protists, and archaea, which are collectively known as the ‘gut microbiota’ (see Glossary) 1, 2. This complex ecosystem exerts a number of highly specialised functions that are essential to host physiology, including the absorption of nutrients, synthesis of essential organic compounds, development of adaptive immunity, and protection against pathogens 3, 4, 5, 6.

Strategies of Acquisition and Maintenance of Helminth Microbiomes

Investigations of the interactions between parasites and their resident bacteria rely on a thorough understanding of the dynamics of microbiome acquisition. Whilst for GI nematodes knowledge in this area is relatively limited, several investigations have documented the fine strategy via which bacteria of the genus Wolbachia are propagated through successive generations of filarial parasites (reviewed in [21]) (cf. Figure 1). In the filarial nematode B. malayi, these bacteria inhabit the lateral

Are Helminth Microbiomes Key to Parasite Fitness?

Studies of the structure and function of helminth microbiomes are in their infancy. Nevertheless, over the past decades, evidence has emerged about the functional association between the free-living nematode Caenorhabditis elegans and the bacteria inhabiting it 31, 32. Indeed, C. elegans is known to host a species-rich bacterial community, dominated by Proteobacteria, such as Enterobacteriaceae and members of the genera Pseudomonas, Stenotrophomonas, Ochrobactrum, and Sphingomonas 31, 32.

New Generation of Helminth Microbiome-Targeting Chemotherapeutics?

Globally, more than two billion people are at risk of infection by GI nematodes, mainly the hookworms Ancylostoma duodenale and Necator americanus, the whipworm T. trichiura, the roundworm Ascaris lumbricoides, and the threadworm, Strongyloides stercoralis. Collectively, these nematodes are responsible for more than 5.5 million disability-adjusted life years (DALYs) (reviewed in [47]). Moreover, GI nematodes inflict significant production losses in livestock due to the extensive morbidity and

Concluding Remarks

In spite of substantial evidence that points towards key role(s) of microbial species inhabiting parasitic helminths in the fundamental biology of these pathogens and host–parasite interactions, for example, in filarial nematodes and, more recently, whipworms, current knowledge of the microbiomes of key parasites of major socioeconomic significance, such as GI nematodes of humans and livestock, is scarce and fragmented. Nonetheless, the relentless progress in microbiome investigation and

Acknowledgments

T.P.J. is the grateful recipient of a PhD scholarship by the Biotechnology and Biological Sciences Research Council (BBSRC) of the UK. Research in the C.C. laboratory is funded by grants by the Isaac Newton Trust, the Isaac Newton Trust/Wellcome Trust/University of Cambridge joint grant scheme and by the Royal Society (UK). Research in the R.B.G. laboratory is supported predominantly by the Australian Research Council (ARC), the National Health and Medical Research Council (NHMRC), Melbourne

Glossary

Core microbiome
the group of microbes consistently found within a host microbiome, which demonstrate a persistent association and provide a critical function within the habitat in which they are detected.
Endosymbiont
any organism that lives within the body or cells of another organism in a symbiotic relationship with the host body or cell, often but not always to mutual benefit.
Helminth microbiome
the collective microbiome of parasitic helminths.
Macrobiota
collective term used to describe the

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