Exploiting the architecture and the features of the microsporidian genomes to investigate diversity and impact of these parasites on ecosystems

Abstract

Fungal species play extremely important roles in ecosystems. Clustered at the base of the fungal kingdom are Microsporidia, a group of obligate intracellular eukaryotes infecting multiple animal lineages. Because of their large host spectrum and their implications in host population regulation, they influence food webs, and accordingly, ecosystem structure and function. Unfortunately, their ecological role is not well understood. Present also as highly resistant spores in the environment, their characterisation requires special attention. Different techniques based on direct isolation and/or molecular approaches can be considered to elucidate their role in the ecosystems, but integrating environmental and genomic data (for example, genome architecture, core genome, transcriptional and translational signals) is crucial to better understand the diversity and adaptive capacities of Microsporidia. Here, we review the current status of Microsporidia in trophic networks; the various genomics tools that could be used to ensure identification and evaluate diversity and abundance of these organisms; and how these tools could be used to explore the microsporidian life cycle in different environments. Our understanding of the evolution of these widespread parasites is currently impaired by limited sampling, and we have no doubt witnessed but a small subset of their diversity.

Figure 1

Simplified schematic representation of trophic networks integrating the microbial loop in pelagic aquatic environments (modified from (Amblard et al., 1998)). All components of the microbial loop are shown in grey. The red asterisks indicate known organisms that are susceptible to Microsporidia parasitism. DOM, dissolved organic matter.

Figure 2

General features and phylogenetic relationships of sequenced microsporidian genomes. Phylogenetic relationships were established based on several analyses (Wang et al., 2006; Corradi et al., 2009; Cuomo et al., 2012; Suankratay et al., 2012).

Figure 3

Impact of TEs on microsporidian genome architectures. (a) Schematic representation of three genome structures observed in the microsporidian species Encephalitozoon cuniculi, Nosema ceranae and Anncaliia algerae. Genes are indicated in yellow boxes, and TEs are indicated in blue boxes. (b) Overview of TEs described in the microsporidian genomes. Information was obtained from both the literature and personal analysis with TransposonPSI (http://transposonpsi.sourceforge.net/).

Figure 4

Schematic representation of the major approaches to appraise Microsporidia diversity in complex environments using microsporidian genomic features.