Beneficial commensal bacteria promote Drosophila growth by downregulating the expression of peptidoglycan recognition proteins

Gallo, Marialaura; Vento, Justin M.; Joncour, Pauline; Quagliariello, Andrea; Maritan, Elisa; Silva-Soares, Nuno F.; Battistolli, Matteo; Beisel, Chase L.; Martino, Maria Elena

doi:10.1016/j.isci.2022.104357

Cited by 11 publications

(4 citation statements)

References 102 publications

(163 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Microbial abundance is thus critical for promoting y growth and development 26,43,49 . At the same time, Drosophila gut microbes are able to actively in uence the host response, by modulating Tor and insulin signaling pathways, promoting intestinal peptidase expression, boosting the immune response, as well as cooperating among them 31,40,41,45,46,[50][51][52][53] . Altogether, these studies demonstrate that microbes possess a dual role in promoting host development.…”

Section: Introductionmentioning

confidence: 99%

Gut microbes predominantly act as symbiotic partners rather than raw nutrients

Soares

Quagliariello

Yigitturk

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Animals and their gut microbes mutually benefit their health. In this frame, nutrition has a central role by directly affecting both host and microbes’ fitness and their effects. This makes nutritional symbioses a complex and dynamic tri-system of diet-microbiota-host. Despite recent discoveries on this field, full control over the interplay among these partners is challenging and hinders the resolution of fundamental questions, such as how to parse the gut microbes’ effect as raw nutrition or as symbiotic partners? To tackle this, we made use of the well-characterized Drosophila melanogaster/Lactiplantibacillus plantarum experimental model of nutritional symbiosis to generate a quantitative framework of gut microbes’ effect on the host. We show that the beneficial effect of L. plantarum strains primarily results from the active relationship as symbionts rather than raw nutrients, regardless of the bacterial strain. Metabolomic analysis of both active and inactive bacterial cells further demonstrated the crucial role of the production of beneficial bacterial metabolites, such as N-acetylated-amino-acids, as result of active bacterial growth and function. Altogether, our results provide a ranking and quantification of the main bacterial features contributing to sustain animal growth. We demonstrate that viability is the predominant and necessary variable involved in bacteria-mediated benefit, followed by strain-specific properties and the nutritional potential of the bacterial cells as direct energy source. This contributes to elucidate the role of beneficial bacteria and probiotics, creating a broad quantitative framework for host-gut microbiome that can be expanded to other model systems.

show abstract

Section: Introductionmentioning

confidence: 99%

Gut microbes predominantly act as symbiotic partners rather than raw nutrients

Soares

Quagliariello

Yigitturk

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Microbial abundance is thus critical for promoting fly growth and development 26,43,49 . At the same time, Drosophila gut microbes are able to actively influence the host response, by modulating Tor and insulin signaling pathways, promoting intestinal peptidase expression, boosting the immune response, as well as cooperating among them 31,40,41,45,46,[50][51][52][53] . Altogether, these studies demonstrate that microbes possess a dual role in promoting host development.…”

Section: Introductionmentioning

confidence: 99%

Gut microbes predominantly act as symbiotic partners rather than raw nutrients

Soares

Quagliariello

Yigitturk

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

Animals and their gut microbes mutually benefit their health. In this frame, nutrition has a central role by directly affecting both host and microbe fitness and their effects. This makes nutritional symbioses a complex and dynamic tri-system of diet-microbiota-host. Despite recent discoveries on this field, full control over the interplay among these partners is challenging and hinders the resolution of fundamental questions, such as how to parse the gut microbes effect as raw nutrition or as symbiotic partners? To tackle this, we made use of the well-characterized Drosophila melanogaster/Lactiplantibacillus plantarum experimental model of nutritional symbiosis to generate a quantitative framework of gut microbe effect on the host. We show that the beneficial effect of L. plantarum strains primarily results from the active relationship as symbionts rather than raw nutrients, regardless of the bacterial strain. Metabolomic analysis of both active and inactive bacterial cells further demonstrated the crucial role of the production of beneficial bacterial metabolites, such as N-acetylated-amino-acids, as result of active bacterial growth and function. Altogether, our results provide a ranking and quantification of the main bacterial features contributing to sustain animal growth. We demonstrate that viability is the predominant and necessary variable involved in bacteria-mediated benefit, followed by strain-specific properties and the nutritional potential of the bacterial cells as direct energy source. This contributes to elucidate the role of beneficial bacteria and probiotics, creating a broad quantitative framework for host-gut microbiome that can be expanded to other model systems.

show abstract

“…Instead of live yeasts, the foods typically contain heat-killed budding yeast Saccharomyces cerevisiae as a major nutrient source, but this yeast species rarely coexists with Drosophila in the wild ( Hoang et al, 2015 ). Consequently, the relationship between Drosophila and its associated microorganisms has often been classified as facultative ( Gallo et al, 2022 ; Martino et al, 2018 ), and the role played by associated fungi has been largely overlooked.…”

Section: Introductionmentioning

confidence: 99%

Identification of key yeast species and microbe–microbe interactions impacting larval growth of Drosophila in the wild

Mure,

Sugiura,

Maeda

et al. 2023

eLife

View full text Add to dashboard Cite

Microbiota consisting of various fungi and bacteria have a significant impact on the physiological functions of the host. However, it is unclear which species are essential to this impact and how they affect the host. This study analyzed and isolated microbes from natural food sources of Drosophila larvae, and investigated their functions. Hanseniaspora uvarum is the predominant yeast responsible for larval growth in the earlier stage of fermentation. As fermentation progresses, Acetobacter orientalis emerges as the key bacterium responsible for larval growth, although yeasts and lactic acid bacteria must coexist along with the bacterium to stabilize this host-bacterial association. By providing nutrients to the larvae in an accessible form, the microbiota contributes to the upregulation of various genes that function in larval cell growth and metabolism. Thus, this study elucidates the core microbial species that support animal growth under microbial transition.

show abstract

Beneficial commensal bacteria promote Drosophila growth by downregulating the expression of peptidoglycan recognition proteins

Cited by 11 publications

References 102 publications

Gut microbes predominantly act as symbiotic partners rather than raw nutrients

Gut microbes predominantly act as symbiotic partners rather than raw nutrients

Gut microbes predominantly act as symbiotic partners rather than raw nutrients

Identification of key yeast species and microbe–microbe interactions impacting larval growth of Drosophila in the wild

Contact Info

Product

Resources

About