Lactobacillus plantarum favors the early emergence of fit and fertile adult Drosophila upon chronic undernutrition

Abstract

Animals are naturally surrounded by a variety of microorganisms with which they constantly interact. Among these microbes, some live in close association with a host and form its microbiota. These communities are being extensively studied, owing to their contributions to shaping various aspects of animal physiology. One of these commensal species, Lactobacillus plantarum, and in particular the L.p.WJL strain, has been shown to promote the growth of Drosophila larvae upon nutrient scarcity, allowing earlier metamorphosis and adult emergence compared with axenic individuals. As for many insects, conditions surrounding the post-embryonic development dictate key adult life history traits in Drosophila, and adjusting developmental timing according to the environment is essential for adult fitness. Thus, we wondered whether the growth acceleration induced by L.p.WJL in a context of poor nutrition could adversely impact the fitness of Drosophila adults. Here, we show that the L.p.WJL-mediated acceleration of growth is not deleterious; adults emerging after an accelerated development are as fit as their axenic siblings. Additionally, the presence of L.p.WJL even leads to a lifespan extension in nutritionally challenged males. These results demonstrate that L.p.WJL is a beneficial partner for Drosophila melanogaster through its entire life cycle. Thus, commensal bacteria allow the earlier emergence and longer survival of fit and fertile individuals and might represent one of the factors contributing to the ecological success of Drosophila.

Mono-Association withLactobacillus plantarumDisrupts Intestinal Homeostasis in adultDrosophila

“…Irrespective of the means used to generate GF flies, we found that Lp significantly shortened the lifespan of adult Drosophila (Figure 2C, E). These observations match a recent report that GF adults outlive flies mono-associated with the WJL strain of Lp (48) and indicate that mono-association of adults with Lp reverts the extended lifespan noted in GF flies. In contrast, mono-association of adult Drosophila with Ap had no effect on adult lifespan regardless of the method used to generate GF flies ( Figure 2D, F).…”

“…In this report, we used the Drosophila model to examine the effects of symbiotic bacteria on the long-term maintenance of the epithelial renewal program. A recent report showed that mono-association with Lp is not deleterious for adult fly fitness, and has benefits for males raised under conditions of nutrient scarcity (48). In this study, we asked if Lp affects ISC division independent of effects on lifespan, as we showed previously that manipulation of ISC division rates does not have substantial effects on lifespan (36).…”

Environmental specificity in Drosophila-bacteria symbiosis affects host developmental plasticity

“…In addition to physical differences between laboratory medium and fresh fruit, the nature and concentration of available nutrient are likely to differ. It is well known that lactic and acetic acid bacteria, two taxa that were not investigated in our experiment, can promote larval growth upon nutrient scarcity (Shin et al 2011;Storelli et al 2011, Téfit et al 2017). However, it is also well established that bacteria can affect Drosophila phenotype through signaling (Storelli et al 2011) as well as nutrient provisioning (Brownlie et al 2009;Bing et al 2018;Sannino et al 2018).…”

“…In this species, bacterial symbionts contribute to a broad range of functions including resource acquisition, digestion, immunity and behavior (Broderick and Lemaitre 2012;Ankrah and Douglas 2018;Schretter et al 2018). Several laboratory studies have established fly nutrition relies on interactions with gut bacteria (Shin et al 2011;Storelli et al 2011;Ridley et al 2012;Wong et al 2014;Huang et al 2015;Leitão-Gonçalves et al 2017;Téfit et al 2017). In particular, bacterial genera frequently associated with laboratory flies, such as Acetobacter and Lactobacillus, can improve larval growth and development when laboratory food is poor in proteins (Shin et al 2011;Storelli et al 2011;Téfit et al 2017).…”

“…Several laboratory studies have established fly nutrition relies on interactions with gut bacteria (Shin et al 2011;Storelli et al 2011;Ridley et al 2012;Wong et al 2014;Huang et al 2015;Leitão-Gonçalves et al 2017;Téfit et al 2017). In particular, bacterial genera frequently associated with laboratory flies, such as Acetobacter and Lactobacillus, can improve larval growth and development when laboratory food is poor in proteins (Shin et al 2011;Storelli et al 2011;Téfit et al 2017). Even though some bacterial taxa are frequent in laboratory colonies, the composition of Drosophila bacterial gut communities largely varies among laboratories (Chandler et al 2011;Staubach et al 2013;Wong et al 2013;Vacchini et al 2017).…”