Linking the effects of helminth infection, diet and the gut microbiota with human whole-blood signatures.

Soo Ching Lee,Joseph Cooper Devlin,Yvonne A L Lim,Foong Ming Moy,Alice V Easton,Tsung Fei Khang,Mei San Tang,Ilseung Cho,Ling Ling Chua,P’Ng Loke,Makedonka Mitreva

doi:10.1371/journal.ppat.1008066

Abstract

Helminth infection and dietary intake can affect the intestinal microbiota, as well as the immune system. Here we analyzed the relationship between fecal microbiota and blood profiles of indigenous Malaysians, referred to locally as Orang Asli, in comparison to urban participants from the capital city of Malaysia, Kuala Lumpur. We found that helminth infections had a larger effect on gut microbial composition than did dietary intake or blood profiles. Trichuris trichiura infection intensity also had the strongest association with blood transcriptional profiles. By characterizing paired longitudinal samples collected before and after deworming treatment, we determined that changes in serum zinc and iron levels among the Orang Asli were driven by changes in helminth infection status, independent of dietary metal intake. Serum zinc and iron levels were associated with changes in the abundance of several microbial taxa. Hence, there is considerable interplay between helminths, micronutrients and the microbiota on the regulation of immune responses in humans.

Highlights

During the course of human evolution, the majority of our ancestors were likely colonized by helminths, as are most mammals in the wild [1]
Parasitic intestinal worms and gut bacteria occupy the same space, but we do not understand the nature and scope of their interaction. This is further complicated by dietary effects on the gut bacteria, as well as the immune responses of the host
During the cross-sectional phase of the study, we first conducted a detailed 7-day nutritional questionnaire among 49 consenting asymptomatic Malaysian indigenous individuals living in a rural setting next to the jungle to determine dietary intake variables

Summary

Introduction

During the course of human evolution, the majority of our ancestors were likely colonized by helminths, as are most mammals in the wild [1]. The heterogeneity in responses to helminths has led to severe morbidity in a proportion of infected individuals [3]. This heterogeneity is poorly understood and could be the result of a complex relationship between host genotype, parasite genotype and the gut microbiota of infected individuals. The most widespread helminth infections in man, as well as in most other mammals, are the intestinal helminths [4,5,6]. This is the locale of the majority of commensal bacteria in mammals. The microbiota can alter the efficacy and toxicity of drugs [15], may impact the pharmacodynamics of deworming treatment

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Conclusion