Microbiome “Inception”: an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host

Abstract

The importance of the parasite microbiome is gaining recognition. Of particular concern is understanding how these parasite microbiomes influence host-parasite interactions and parasite interactions with the vertebrate host microbiome as part of a system of nested holobionts.

Eco-evolutionary implications of helminth microbiomes

“…For example, the composition of the human microbiome has been linked to gut health, immunity modulation and disease susceptibility (Wang et al, 2017;Fassarella et al, 2021); the taste of wine has been linked to microbial communities in the soil (Belda et al, 2017); and in conservation programmes, the health status of captivity-bred species has been linked to differences in the microbiome composition between their natural and artificial habitats (West et al, 2019). Similarly, symbiotic microbes are also present in helminth parasites and their parasitized hosts, performing central roles in what was previously seen as a two-player interaction (parasitehost), with eco-evolutionary implications for all players involved (Morley, 2016;Dheilly et al, 2019b;Jenkins et al, 2019;Brealey et al, 2022;Hahn et al, 2022;Poulin et al, 2022).…”

“…Among parasites, helminths are ubiquitous in the terrestrial and marine environment and are especially interesting from an evolutionary perspective, with their many different life stages requiring a combination of invertebrate and vertebrate hosts to complete a life cycle (Bennett et al, 2021(Bennett et al, , 2022. Microbes in direct symbiosis with organisms parasitized by helminths have been reviewed elsewhere and perform many roles, including resistance to the parasites, heat tolerance, diet supplementation, development and immune defence (Dheilly et al, 2015;Reynolds et al, 2015;Brealey et al, 2022). Helminths are economically relevant pathogens to vertebrates, which may be the reason why research at the parasitized organism level usually focuses on the effect of specific microbes on the susceptibility, infection, or resistance of the parasitized organism to the parasite.…”

“…In many instances, bacterial taxa composing microbial communities are variable even among helminths parasitizing the same individual host (Jorge et al, 2020(Jorge et al, , 2022bHahn et al, 2022), and, when disrupted with antibiotics, increased abundance of founder bacteria postdisturbance may follow (Jorge et al, 2022c). In other cases, there is little diversity in the bacteria composing helminth microbiomes (Brealey et al, 2022). The impact of these phenomena on the fitness and evolution of helminths is still unclear.…”

“…Thus, a parasite's bacteriome is not simply a random assemblage of the pool of bacteria available in the parasite's habitat, as natural selection may restrict which bacteria will successfully colonize the helminth, although it may also depend on which bacteria were settled in before (Hahn et al, 2022;Jorge et al, 2022bJorge et al, , 2022c. Interestingly, Eubothrium cestodes parasitizing salmon were shown to associate with different Mycoplasma lineages than those found in the salmon`s microbiome, suggesting a role of divergent selection for specific Mycoplasma lineages in the cestode parasite and its salmon host (Brealey et al, 2022). Yet, the Mycoplasma lineages associated with the cestode and the salmon are phylogenetically very close, suggesting shared ancestry of the specific bacterial lineages between the salmon and cestode (Brealey et al, 2022).…”

“…Recent work has revealed that the microbiome within different helminths can range from very simple (with only a few conserved taxa associated with multiple individual helminths of the same population) to highly complex (with several different taxa and significant variability in community composition among individuals) (Hahn et al , 2022; Jorge et al , 2022a). Helminth microbiomes can influence infection success and susceptibility to the host's immune responses (Dheilly et al , 2015; Martinson et al , 2020; Brealey et al , 2022), and may play a role in the ability of some manipulative parasites to alter the phenotype of their animal hosts (Poulin et al , 2022). A helminth species may have a geographically variable microbiome (Jorge et al , 2022b), but specific microbiome components may be consistent over the many life stages of the parasite's life cycle (Jorge et al , 2020).…”