Caenorhabditis elegans as a Model for Microbiome Research

Abstract

The nematode Caenorhabditis elegans is used as a central model system across biological disciplines. Surprisingly, almost all research with this worm is performed in the absence of its native microbiome, possibly affecting generality of the obtained results. In fact, the C. elegans microbiome had been unknown until recently. This review brings together results from the first three studies on C. elegans microbiomes, all published in 2016. Meta-analysis of the data demonstrates a considerable conservation in the composition of the microbial communities, despite the distinct geographical sample origins, study approaches, labs involved and perturbations during worm processing. The C. elegans microbiome is enriched and in some cases selective for distinct phylotypes compared to corresponding substrate samples (e.g., rotting fruits, decomposing plant matter, and compost soil). The dominant bacterial groups include several Gammaproteobacteria (Enterobacteriaceae, Pseudomonaceae, and Xanthomonodaceae) and Bacteroidetes (Sphingobacteriaceae, Weeksellaceae, Flavobacteriaceae). They are consistently joined by several rare putative keystone taxa like Acetobacteriaceae. The bacteria are able to enhance growth of nematode populations, as well as resistance to biotic and abiotic stressors, including high/low temperatures, osmotic stress, and pathogenic bacteria and fungi. The associated microbes thus appear to display a variety of effects beneficial for the worm. The characteristics of these effects, their relevance for C. elegans fitness, the presence of specific co-adaptations between microbiome members and the worm, and the molecular underpinnings of microbiome-host interactions represent promising areas of future research, for which the advantages of C. elegans as an experimental system should prove of particular value.

The Natural Biotic Environment ofCaenorhabditis elegans

“…Importantly, C. elegans -associated communities from the two very distinct study approaches are highly similar, including enrichment of eight particular families across the two studies, such as Enterobacteriaceae , Pseudomonaceae , Xanthomonadacea e, Comamonadaceae , Sphingomonadaceae , Sphingobacteriaceae , Weeksellaceae , and Flavobacteriaceae (Zhang et al 2017). In spite of these recent advances, it is yet unclear how stable the C. elegans -associated microbiome really is, either during the lifetime of individuals or across host generations.…”

A peek into the microbiome of two free-living aquatic nematodes Anticoma & Daptonema

“…The third is the marine nematodes with chemoautotrophic or methanotrophic bacteria, which are studied for their unique associations enabling them to take advantage of the different metabolic pathways available to their symbionts [8,9,10] . The remaining, relatively limited studied, focus on plant parasitic and free-living nematodes and their associated bacteria [11,12,13,14] . Of these the most recent additions are the exploration of the microbiome of free-living nematode Litoditis marina complex by Derycke et al [15] and the most comprehensive look at the microbiome of the model species -Caenorhabditis elegans (Maupas) [12,13,14] .…”

“…The remaining, relatively limited studied, focus on plant parasitic and free-living nematodes and their associated bacteria [11,12,13,14] . Of these the most recent additions are the exploration of the microbiome of free-living nematode Litoditis marina complex by Derycke et al [15] and the most comprehensive look at the microbiome of the model species -Caenorhabditis elegans (Maupas) [12,13,14] . The extensive data accrued on C. elegans has opened unprecedented opportunities to explore the role of associated microbiome on nematode fitness using genetic tools.…”

“…The extensive data accrued on C. elegans has opened unprecedented opportunities to explore the role of associated microbiome on nematode fitness using genetic tools. The limited look at microbiome of this model species has already revealed that individuals of this species isolated from seemingly unrelated and dissimilar habitats from distant geographic locations harbored a distinct signature microbiome commonly [14] . Available data also shows that some microbes help with host immunity and help protect nematodes from infective bacteria and fungi, while others enhance growth and reproduction.…”

“…Yokouchi et al [19] and Martinez-Garcia et al [20] have also used (MDA) in a marine environment as a pre-PCR step to address these issues and aid in identifying bacterial associations with coral [19] and protists [20] respectively. We recognize that these recent works [12,13,14,15] employ molecular tools most appropriate in that they provide a relatively more comprehensive information on the microbial communities. We, however, also recognize that in the absence of high throughput marker gene-based metagenomic sequencing, a combination of methods including multiple displacement amplification (MDA) followed by PCR, and denaturing gradient gel electrophoresis (DGGE) using marker genes provide useful information on the microbiome of these little explored free-living nematodes.…”