The eukaryome: Diversity and role of microeukaryotic organisms associated with animal hosts

Abstract

Abstract Awareness of the roles that host‐associated microbes play in host biology has escalated in recent years. However, microbiome studies have focused essentially on bacteria, and overall, we know little about the role of host‐associated eukaryotes outside the field of parasitology. Despite that, eukaryotes and microeukaryotes in particular are known to be common inhabitants of animals. In many cases, and/or for long periods of time, these associations are not associated with clinical signs of disease. Unlike the study of bacterial microbiomes, the study of the microeukaryotes associated with animals has largely been restricted to visual identification or molecular targeting of particular groups. So far, since the publication of the influential Human Microbiome Project Consortium paper in 2012, few studies have been published dealing with the microeukaryotes using a high‐throughput barcoding ‘microbiome‐like’ approach in animals. Nonetheless, microeukaryotes have an impact on the host physiology and lifestyle and also on the diversity and composition of the wider symbiotic community of bacteria and viruses. Beyond being parasites, microeukaryotes have many different roles in animals. For example, they directly interact with the host immune system in mammals; they have a key role on cellulose degradation, lignocellulose in xylophage termites and cockroaches; and they have an essential role in providing photosynthates to reef‐building corals. Certain microeukaryotic lineages have diversified within hosts more than others. These cases of co‐evolution led to different forms of symbiosis: from mutualism (like Symbiodinium in corals or parabasalians in termites), to commensalism (Blastocystis in humans) or to strict parasitism (apicomplexans or microsporidians in a broad range of hosts). We will review the ecological context and the evolutionary mechanisms that ended up in these different symbiotic scenarios, across the taxonomic range of both symbionts and their metazoan hosts. Host‐associated microeukaryotes have impacts at many levels, from individual animal health to ecosystems and to agroeconomy. Therefore, it is crucial to have a better understanding of their diversity and roles. Novel methodologies are being developed to access the eukaryotic fraction of the microbiome using high‐throughput methods. From ‐omics, to imaging and barcoding approaches biased against metazoans, these novel methodologies and strategies are helping us to increase and improve our knowledge of microeukaryotes in animal‐associated environments. A free Plain Language Summary can be found within the Supporting Information of this article.