The Enterocytozoonidae: the emergence of a microsporidian clade into the aquatic and terrestrial food-chain

Abstract

Pathogens of livestock have proven to be a major concern, in terms of human health, economic sustainability and food availability. They have been shown to be a limiting factor in regard to these three factors and, as such, will become a growing problem as the global population continues to expand. Controlling and predicting pathogen outbreaks is vital to the sustained growth of populations and has become an important topic of study. However, it is a complex process with a multitude of varying factors, that cannot be solved through one method. A specific family of Microsporidia, the Enterocytozoonidae, has received a lot of attention in regard to their effect on human health and aquaculture. Enterocytozoonids are largely found in marine environments and mainly infect aquatic hosts. Many of the organisms infected by enterocytozoonids are economically important to aquaculture, with a number infecting wild-caught fish and farmed crustacea. Two species, in particular, have received a lot of academic and medical attention, Enterocytozoon bieneusi and Enterocytozoon hepatopenaei. However, the family as a whole is understudied and the diversity described is hypothesised not to be a true representation of the family’s diversity or distribution. The aim of this thesis is to assess the potential risk the Enterocytozoonidae have on aquaculture. This has been done in three different ways: i) it described and catalogued the current diversity and distribution in South West UK estuaries and a greater spatial scale using metagenomic databases, ii) using population genomics, it investigates the biogeography of, E. hepatopenaei, a pathogen of two shrimp (Penaeus vannamei and Penaeus monodon) widely farmed in South East Asia, with the aim to infer transmission routes into shrimp ponds, iii) and lastly, it investigated the loss and gain of orthogroups within the Enterocytozoonidae associated with the lineage wide host-shift to aquatic host from terrestrial hosts. Overall, this thesis found a greater distribution and abundance for Enterospora canceri and E. hepatopenaei in the locations sampled, and greater diversity within the Enterocytozoondiae than was previously described. Suggesting an alternative host (s) for En. canceri, likely planktonic crustacea, as prevalence in the current described host was very low (3%). Use of metagenomic databases in this study also expanded upon the known distribution and diversity of the Enterocytozoonidae, showing a largely marine-based distribution. Suggesting an Atlantic-based radiation. It found that E. hepatopenaei is likely to be endemic to the countries examined, due to strong geographic signals. However, analysis suggests some transmission between Thailand India and China. Lastly, it identified candidate genes, unique to lineages within the Enterocytozoonidae, that could contribute to the family’s success in the invasion of their respective host cells. A greater diversity and abundance for novel sequences more related to the Enterocytozoon/Enterospora branch of the Enterocytozoondiae was also observed, suggesting, at least in estuaries in the Southwest of the United Kingdom, that this clade may be more diverse. Possibly due to their described main hosts being planktonic crustaceans. Which may lend to the success of the two most prevalent species in the family, E. hepatopenaei and E. bieneusi. This study found that the Enterocytozoonidae likely pose a continued threat to aquatic livestock, largely due to their widespread nature, overlapping with human influenced environments, and evident opportunistic propensity to host-shift. In addition, also being present inland in freshwater makes preventative measures difficult, as they could be found in a range of water sources.