Drosophila melanogaster establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria

Autor:	Marta Sporniak, Rita S Valente, Ines Silva Pais, Luis Augusto Teixeira
Rok vydání:	2018
Předmět:	0301 basic medicine Gut flora Biochemistry Melanogaster Biology (General) Axenic Genetics Mutualism (biology) 0303 health sciences education.field_of_study biology Drosophila Melanogaster General Neuroscience Eukaryota Agriculture Animal Models Biodiversity Insects Nucleic acids Experimental Organism Systems Ribosomal RNA Drosophila Female Drosophila melanogaster General Agricultural and Biological Sciences Research Article Cell biology Cellular structures and organelles Arthropoda QH301-705.5 Population Zoology Crops Research and Analysis Methods Models Biological General Biochemistry Genetics and Molecular Biology 03 medical and health sciences Model Organisms Species Specificity Animals Adults Non-coding RNA Symbiosis education 030304 developmental biology Bacteria General Immunology and Microbiology 030306 microbiology Gut Bacteria fungi Organisms Biology and Life Sciences biology.organism_classification Invertebrates Gastrointestinal Microbiome Gastrointestinal Tract Lactobacillus 030104 developmental biology Age Groups People and Places RNA Population Groupings Acetobacter Ribosomes Crop Science
Zdroj:	PLOS Biology PLoS Biology, Vol 16, Iss 7, p e2005710 (2018) PLoS Biology
ISSN:	1545-7885
DOI:	10.1371/journal.pbio.2005710
Popis:	Animals live together with diverse bacteria that can impact their biology. In Drosophila melanogaster, gut-associated bacterial communities are relatively simple in composition but also have a strong impact on host development and physiology. It is generally assumed that gut bacteria in D. melanogaster are transient and their constant ingestion with food is required to maintain their presence in the gut. Here, we identify bacterial species from wild-caught D. melanogaster that stably associate with the host independently of continuous inoculation. Moreover, we show that specific Acetobacter wild isolates can proliferate in the gut. We further demonstrate that the interaction between D. melanogaster and the wild isolated Acetobacter thailandicus is mutually beneficial and that the stability of the gut association is key to this mutualism. The stable population in the gut of D. melanogaster allows continuous bacterial spreading into the environment, which is advantageous to the bacterium itself. The bacterial dissemination is in turn advantageous to the host because the next generation of flies develops in the presence of this particularly beneficial bacterium. A. thailandicus leads to a faster host development and higher fertility of emerging adults when compared to other bacteria isolated from wild-caught flies. Furthermore, A. thailandicus is sufficient and advantageous when D. melanogaster develops in axenic or freshly collected figs, respectively. This isolate of A. thailandicus colonizes several genotypes of D. melanogaster but not the closely related D. simulans, indicating that the stable association is host specific. This work establishes a new conceptual model to understand D. melanogaster–gut microbiota interactions in an ecological context; stable interactions can be mutualistic through microbial farming, a common strategy in insects. Moreover, these results develop the use of D. melanogaster as a model to study gut microbiota proliferation and colonization. Author summary Animals, including humans, live together with complex bacterial communities in their gut that influence their physiology and health. The fruit fly Drosophila melanogaster is an excellent model organism to study host–microbe interactions and harbors a relatively simple gut bacterial community. The dominating hypothesis in the field is that gut bacteria in D. melanogaster are unstable and their constant ingestion with food is required to maintain their levels in the gut. Here, however, we show in D. melanogaster collected from a natural population, that stable gut bacteria do exist. We isolated specific species that can proliferate in the gut and form a stable association that is beneficial for both the bacteria and the flies. For the bacteria, they benefit from being constantly disseminated by the flies as they move around. For the flies, this is a form of farming, as the next generation of flies benefits from the association with these particular bacteria during development. Flies associated with these bacteria during the larval stages become adults faster and are more fertile than if they develop with other bacteria encountered in nature. Our findings show that D. melanogaster has stable colonizing bacteria in the gut, which are important for host development, establishing a new framework to study host–gut bacteria interactions.
Databáze:	OpenAIRE
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