Combining morphology, behaviour and genomics to understand the evolution and ecology of microbial eukaryotes

Abstract

Microbial eukaryotes (protists) are structurally, developmentally and behaviourally more complex than their prokaryotic cousins. This complexity makes it more difficult to translate genomic and metagenomic data into accurate functional inferences about systems ranging all the way from molecular and cellular levels to global ecological networks. This problem can be traced back to the advent of the cytoskeleton and endomembrane systems at the origin of eukaryotes, which endowed them with a range of complex structures and behaviours that still largely dominate how they evolve and interact within microbial communities. But unlike the diverse metabolic properties that evolved within prokaryotes, the structural and behavioural characteristics that strongly define how protists function in the environment cannot readily be inferred from genomic data, since there is generally no simple correlation between a gene and a discrete activity or function. A deeper understanding of protists at both cellular and ecological levels, therefore, requires not only high-throughput genomics but also linking such data to direct observations of natural history and cell biology. This is challenging since these observations typically require cultivation, which is lacking for most protists. Potential remedies with current technology include developing a more phylogenetically diverse range of model systems to better represent the diversity, as well as combining high-throughput, single-cell genomics with microscopic documentation of the subject cells to link sequence with structure and behaviour. This article is part of a discussion meeting issue 'Single cell ecology'.

Keywords: behaviour; ecology; eukaryotic; evolution; genomics; protist.

Figure 1.

Tree of eukaryotes. A schematic tree summarizing current data on the relationships between major lineages of eukaryotes with selected ancient and recent examples of structural complexity and behaviour. Examples of basic behaviours (and complex behaviours emerging from them) are indicated at the root of the tree, and are predicted to be present in the last eukaryotic common ancestor (LECA). These include (left to right) gliding motility, ontogenetic development, phagocytosis, amoeboid movement, forming endosymbiotic associations and flagellar swimming. These have all existed since the LECA or soon after, and in some cases, all modern examples are homologous (e.g. flagella), whereas others are constantly reinvented in parallel (e.g. forming endosymbiotic associations or gliding motility). Indicated around the branches of the tree are selected examples of complex structures and behaviours (often resulting from strings of basic behaviours) that emerged many times in parallel. These include (left to right) creating cell walls or armour (by aggregating material, crystalization or scaffolding organic material either inside the cell or by secretion), building and expelling extrusomes, intracellular infection, sensory organelles (light sensing eye spots is shown as an example), structural complexity though symmetrical repetition and colony formation (by reproduction or aggregation). These traits have originated many times throughout the evolution of eukaryotes. (Online version in colour.)

Figure 2.

Examples of eukaryotic behaviours, structures and functional coordination between them. Some basic cell behaviours that are common to many or all eukaryotes are shown at the top, and under each example structures associated with that behaviour are indicated. Where more than one structure is listed, structures might all work together to effect the behaviour, or alternatively in different systems different structures are associated with the behaviour. The bottom panel provides examples of complex processes that can result from coordination of these behaviours and structures with other systems (with an emphasis on processes that are most directly affected by the behaviour). This is not a comprehensive summary, but rather a few examples selected to present a range of complexity, age and functional effects. (Online version in colour.)