Adult schistosomes have an epithelial bacterial population distinct from the surrounding mammalian host blood

Abstract

Background Schistosomiasis is a neglected tropical parasitic and chronic disease affecting hundreds of millions of people. Adult schistosomes reside in the blood stream of the definitive mammalian host. These helminth parasites possess two epithelial surfaces, the tegument and the gastrodermis, both of which interact with the host during immune evasion and in nutrient uptake. Methods Female ARC Swiss mice (4–6 weeks old) were infected percutaneously with Schistosoma japonicum cercariae freshly shed from Oncomelania hupensis quadrasi snails (Philippines strain). Fluorescent in situ hybridisation (FISH) was performed by using fresh adult S. japonicum perfused from those infected mice. Adult S. japonicum worms were processed to isolate the tegument from the carcass containing the gastrodermis; blood and bile were collected individually from infected and uninfected mice. Total DNA extracted from all those samples were used for microbiome profiling. Results FISH and microbiome profiling showed the presence of bacterial populations on two epithelial surfaces of adult worms, suggesting they were distinct not only from the host blood but also from each other. Whereas microbial diversity was reduced overall in the parasite epithelial tissues when compared with that of host blood, specific bacterial taxa, including Anoxybacillus and Escherichia, were elevated on the tegument. Minimal differences were evident in the microbiome of host blood during an active infection, compared with that of control uninfected blood. However, sampling of bile from infected animals identified some differences compared with controls, including elevated levels of Limnohabitans, Clostridium and Curvibacter. Conclusions Using FISH and microbial profiling, we were able to demonstrate, for the first time, that bacteria are presented on the epithelial surfaces of adult schistosomes. These schistosome surface-associated bacteria, which are distinct from the host blood microenvironment, should be considered as a new and important component of the host-schistosome interaction. The importance of individual bacterial species in relation to schistosome parasitism needs further elucidation.

High level of C3 is associated with Th2 immune response and liver fibrosis in patients with schistosomiasis

“…Complement proteins in the blood attack pathogens through a series of reactions such as creating pores in the plasma membrane of target organism. 14 Due to the huge pressure of host complement system on the evolution of pathogens, parasites and other microorganisms have developed a set of corresponding mechanisms to escape from complement attack and inhibit complement activity, so as to maintain their survival in the host and the corresponding blood supply. 15 This mechanism is usually achieved by the pathogen avoiding the recognition of complement activator or expressing complement inhibitor.…”

Eco-evolutionary implications of helminth microbiomes

“…Currently, partial 16S rRNA metagenomics is the most used approach to characterize the bacteriome of helminths; it has contributed to revealing that the composition of the bacteriome associated with helminths is different from that associated with the organisms that they parasitize (White et al , 2018; Hogan et al , 2019; Jorge et al , 2020, 2022b, 2022c; Gobert et al , 2022; Hahn et al , 2022), identifying vertical and horizontal transmission of bacterial lineages among helminths (Vandekerckhove et al , 2000; Vaughan et al , 2012; Greiman et al , 2013; Jorge et al , 2020, 2022b; Hahn et al , 2022), and discovering pathogenic bacteria that use helminths as vectors (Pusterla et al , 2003; Greiman et al , 2013; Dheilly et al , 2019a). Partial 16S sequencing has been useful in finding bacteria that are strictly vertically transmitted and in mutualistic associations with helminths (Greiman et al , 2013; Martinson et al , 2020), defining a core bacteriome in a few helminths (Sinnathamby et al , 2018; Jorge et al , 2020, 2022b), and revealing great diversity in the composition and abundance of specific bacterial taxa (Palomares-Rius et al , 2016; Mafuna et al , 2021).…”

Helminth-host-environment interactions: Looking down from the tip of the iceberg

“…Bacteria have been found in the tegument and gastrodermis of digeneans (LoVerde et al 1980; Gobert et al 2022) and tapeworms (see Morley 2016). For example, Salmonella typhimurium replicate within the S. mansoni tegument where they are protected from antibiotics.…”

“…This may account for cases of septicemia following praziquantel treatment of schistosomiasis (LoVerde et al 1980; Barnhilll et al 2011). Bacterial diversity and abundance within S. japonicum differ from that of the blood of the infected host (Gobert et al 2022). A mutually beneficial association seems to exist in that the higher abundance of facultative anaerobes such as Proteobacteria in schistosomes may be associated with the oxygen available in the microenvironment of the worms, and S. japonicum may benefit from a higher abundance of Escherichia coli that reduces adherence of immune molecules to the tegument (Gobert et al 2022).…”

“…Bacterial diversity and abundance within S. japonicum differ from that of the blood of the infected host (Gobert et al 2022). A mutually beneficial association seems to exist in that the higher abundance of facultative anaerobes such as Proteobacteria in schistosomes may be associated with the oxygen available in the microenvironment of the worms, and S. japonicum may benefit from a higher abundance of Escherichia coli that reduces adherence of immune molecules to the tegument (Gobert et al 2022). Adult Fasciola hepatica in sheep have a novel Neorickettsia bacteria that is found in reproductive tissues and in mature eggs within the host liver, raising the possibility that this bacterium may be vertically transmitted within Fasciola (McNulty et al 2017).…”