Towards an integrated understanding of gut microbiota using insects as model systems
Introduction
Extracting essential nutritious components from food can be challenging. Metazoans have partly faced this challenge by forming symbioses with microorganisms that both synthesize essential nutritional compounds and increase the efficiency of nutrient digestion and absorption (Fraune and Bosch, 2010, Moran, 2007). In insects, nutritional symbioses can be split into two main categories: (i) intracellular associations, which are generally found in arthropods with restricted diets such as blood and plant sap and involve only few types of symbionts; and (ii) extracellular associations, that are more common among metazoans and involve a complex community of symbionts that generally live within the gut lumen. Symbionts can serve a range of nutritional functions, from mobilizing stored nitrogen to contributing essential amino acids (Brune and Ohkuma, 2011, Douglas, 2009, Feldhaar, 2011, Kaufman and Klug, 1991), and hosts often rely on symbiotic microorganisms to supply nutrients required for viability and fertility (Dillon and Dillon, 2003, Douglas, 2010, Moran and Baumann, 2000).
In recent decades, numerous investigations have been devoted to understanding the metabolic roles of associated microorganisms (Douglas, 2009, Moran, 2007) with a particular emphasizes on the bacteria that compose the gut microbiota (Dillon and Dillon, 2003, Nicholson et al., 2012, Ryu et al., 2008, Storelli et al., 2011). In this context, it has been shown, for instance, that the gut microbiota can contribute up to 70% of a vertebrate’s energy needs (Flint et al., 2008). However, despite the growing awareness that microbes play key roles in metabolism, health and development of metazoans (Fraune and Bosch, 2010, Lee and Brey, 2013, Maslowski and Mackay, 2011), symbiotic relationships within the gut are far from fully understood (Engel and Moran, 2013).
Perhaps the most important obstacle to understanding these symbiotic relationships resides in the high diversity of bacterial communities living within the gut of most vertebrates. In this regard, insects, which generally harbour a lower microbial diversity within their gut, offer an interesting alternative to vertebrates and have recently emerged as potential model systems to study these interactions. Insects are not only tractable and easy to manipulate, they also offer substantial genetic resources allowing investigations of conversed metabolic and immune pathways. However, capturing the properties of insect gut microbiota has been challenging so far due to a high variability in composition between individuals and closely related species. Here, we give a brief overview of the characteristics of the bacterial communities inhabiting the gut of insects in terms of low diversity but high variability at intra- and interspecific levels and we investigate some of the ecological and methodological factors that might explain such variability. We then emphasize how studies integrating the latest technological advances from molecular biology and stable isotope-based techniques can improve our understanding of host/symbiont interactions.
Section snippets
A low diversity
In contrast to mammals, the bacterial diversity in insect digestive tracts is generally low and rarely exceeds a few tens of species (Colman et al., 2012). In Drosophila, the gut only contains 2–20 bacterial species in natural and/or field conditions (Apidianakis and Rahme, 2011, Bae et al., 2010, Blum et al., 2013, Chandler et al., 2011, Corby-Harris et al., 2007, Cox and Gilmore, 2007, Ren et al., 2007, Ryu et al., 2008, Storelli et al., 2011, Wong et al., 2011), while in humans the gut
Towards an integrated understanding of gut microbiota: from genes to function
Molecular techniques that have been employed to analyse gut microbiota might also be sources of variability, particularly for taxonomic identification. The integration of studies combining different methods might allow a better understanding of individual and communal roles of bacteria in the physiology and ecology of the host.
Conclusion
There is a growing interest in using model systems to provide a comprehensive and integrated understanding of the functioning of the gut microbiota and its interactions with host metabolism and immunity. Insects are relevant systems in many ways (Apidianakis and Rahme, 2011, Charroux and Royet, 2012, Erkosar et al., 2013) and numerous studies already provide an abundance of data on the taxonomic diversity of gut microbiota, but also the ecological factors that might influence this diversity and
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