Host Species and Environmental Effects on Bacterial Communities Associated with Drosophila in the Laboratory and in the Natural Environment

Staubach, Fabian; Baines, John F.; Künzel, Sven; Bik, Elisabeth M.; Petrov, Dmitri A.

doi:10.1371/journal.pone.0070749

Cited by 223 publications

(286 citation statements)

References 58 publications

(127 reference statements)

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“…2A), and this is likely a consequence of all fly lines being inoculated with the same set of microbes at the same starting density. Host genotype likely accounts for a lower proportion of the variation in conventional flies in laboratory culture and wild populations, where the gut microbiota community composition can be influenced by the availability of bacteria in the external environment (14)(15)(16). Full understanding of the determinants of gut microbiota composition will require integration of these multiple genetic, physiological, and ecological factors.…”

Section: Discussionmentioning

confidence: 99%

“…A nutritionally important component of the Drosophila microbiota is the gut-inhabiting bacteria, including members of the Acetobacteraceae (alphaproteobacteria), Lactobacillales, and gammaproteobacteria (14)(15)(16), which contribute to the B vitamin and protein nutrition of the host, and can reduce energy storage as triglyceride (TAG) and glycogen (9,(17)(18)(19). The Drosophila model is also supported by a wealth of genetic and genomic resources, including the Drosophila Genetic Reference Panel (DGRP) comprising multiple inbred lines with sequenced genomes used in this study (20,21).…”

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confidence: 99%

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Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Chaston

Dobson

Newell

et al. 2016

Appl Environ Microbiol

127

131

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A wealth of studies has demonstrated that resident microorganisms (microbiota) influence the pattern of nutrient allocation to animal protein and energy stores, but it is unclear how the effects of the microbiota interact with other determinants of animal nutrition, including animal genetic factors and diet. Here, we demonstrate that members of the gut microbiota in Drosophila melanogaster mediate the effect of certain animal genetic determinants on an important nutritional trait, triglyceride (lipid) content. Parallel analysis of the taxonomic composition of the associated bacterial community and host nutritional indices (glucose, glycogen, triglyceride, and protein contents) in multiple Drosophila genotypes revealed significant associations between the abundance of certain microbial taxa, especially Acetobacteraceae and Xanthamonadaceae, and host nutritional phenotype. By a genome-wide association study of Drosophila lines colonized with a defined microbiota, multiple host genes were statistically associated with the abundance of one bacterium, Acetobacter tropicalis. Experiments using mutant Drosophila validated the genetic association evidence and reveal that host genetic control of microbiota abundance affects the nutritional status of the flies. These data indicate that the abundance of the resident microbiota is influenced by host genotype, with consequent effects on nutrient allocation patterns, demonstrating that host genetic control of the microbiome contributes to the genotype-phenotype relationship of the animal host.T he recognition that animals are routinely colonized by dense and often diverse communities of microorganisms is driving a major reassessment of fundamental aspects of animal biology (1). Notably, there is accumulating evidence that resident microorganisms influence the nutritional status of animals in multiple ways, including competition for ingested nutrients, providing supplementary nutrients (e.g., vitamins, short-chain fatty acids, essential amino acids), and by modulating the nutrient signaling circuits that regulate nutrient allocation (2-5). These discoveries demonstrate the inadequacy of traditional explanations of animal nutrition in terms of nutritional inputs (amount and composition of food ingested) and outputs (animal nutritional demand for activity, growth, reproduction, etc.) and highlight our ignorance of how microbial effects on animal nutrition interact with other factors, especially animal genotype (6-10).The focus of this study is the impact of interactions between the gut microbiota and host genotype on animal nutrition. The nutritional consequence of the microbiota is known to vary with the abundance and composition of the microorganisms (7, 10-13). For example, comparison of nutritional phenotypes in Drosophila melanogaster raised with or without gut bacteria revealed that the microbiome can influence penetrance of host mutations (12). To the extent that the abundance and composition of the microbiota are determined by host genotype, the impact of animal genetic ...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Chaston

Dobson

Newell

et al. 2016

Appl Environ Microbiol

127

131

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“…The experiments were conducted on the association between Drosophila melanogaster fruit flies and their gut microbiota. Natural populations of D. melanogaster consume microorganisms associated with rotting fruit, including various yeasts and bacteria of the Acetobacteraceae and Lactobacillales taxa, and the flies mediate the dispersal of the bacteria via their feces (14)(15)(16)(17). In laboratory culture, all life stages of Drosophila (eggs, larvae, pupae, and adults) are cohoused in vials of agar-based food, enabling precise quantification and manipulation of the microorganisms that cycle between the food and the Drosophila hosts (18)(19)(20)(21).…”

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confidence: 99%

The Host as the Driver of the Microbiota in the Gut and External Environment of Drosophila melanogaster

Wong

Luo

Jing

et al. 2015

Appl Environ Microbiol

120

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Most associations between animals and their gut microbiota are dynamic, involving sustained transfer of food-associated microbial cells into the gut and shedding of microorganisms into the external environment with feces, but the interacting effects of host and microbial factors on the composition of the internal and external microbial communities are poorly understood. This study on laboratory cultures of the fruit fly Drosophila melanogaster reared in continuous contact with their food revealed timedependent changes of the microbial communities in the food that were strongly influenced by the presence and abundance of Drosophila. When germfree Drosophila eggs were aseptically added to nonsterile food, the microbiota in the food and flies converged to a composition dramatically different from that in fly-free food, showing that Drosophila has microbiota-independent effects on the food microbiota. The microbiota in both the flies that developed from unmanipulated eggs (bearing microorganisms) and the associated food was dominated by the bacteria most abundant on the eggs, demonstrating effective vertical transmission via surface contamination of eggs. Food coinoculated with a four-species defined bacterial community of Acetobacter and Lactobacillus species revealed the progressive elimination of Lactobacillus from the food bearing few or no Drosophila, indicating the presence of antagonistic interactions between Acetobacter and Lactobacillus. Drosophila at high densities ameliorated the Acetobacter/Lactobacillus antagonism, enabling Lactobacillus to persist. This study with Drosophila demonstrates how animals can have major, coordinated effects on the composition of microbial communities in the gut and immediate environment. F rom a microbiological perspective, an animal is a transient, nutrient-rich patch. The capacity of various microorganisms to exploit the animal habitat involves multiple traits, including mechanisms that evade or modulate the animal immune system (1-3) and metabolic adaptations to utilize host resources (4, 5). Animal-associated microorganisms include pathogens, whose fitness is coupled to host disease and debility, and beneficial forms that variously contribute nutrients, confer protection, and deliver effectors that promote host performance (6). Consequently, the composition of animal-associated microorganisms is an important determinant of animal fitness.Many animal-microbe associations are open systems, meaning that external microorganisms have access to the host habitat and members of the host microbiota are released back to the external environment via feces, sloughed skin, fluid secretions, etc. (7). Open symbioses can be invaded by external microorganisms that are compatible with the host and are competitive with resident microbiota. As a result, the host is potentially more exposed to parasites and cheats than in a closed system but also has an enhanced capacity to modify the composition of its microbiota adaptively to changes in environmental circumstances (8, 9). The shedding of ...

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“…SK1 and SK3 were also isolated from the midgut of non-TG-RNAi flies. Acetobacter-dominated gut microbiota of Drosophila has been reported, and multiple factors could contribute to the establishment of the composition of microbiota, such as environmental circumstances, compatibility of bacteria, and transmission of bacteria from mother flies to their offspring (28,30,36). SK1 exhibited the strongest resistance against IMD-AMPs, including Cecropin A1 and Diptericin, and ROS, compared with the other three isolated bacteria (Figs.…”

Section: Discussionmentioning

confidence: 99%

RNA Interference Directed against the Transglutaminase Gene Triggers Dysbiosis of Gut Microbiota in Drosophila

Sekihara¹,

Shibata²,

Hyakkendani

et al. 2016

Journal of Biological Chemistry

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Edited by Luke O'NeillWe recently reported that transglutaminase (TG) suppresses immune deficiency pathway-controlled antimicrobial peptides (IMD-AMPs), thereby conferring immune tolerance to gut microbes, and that RNAi of the TG gene in flies decreases the lifespan compared with non-TG-RNAi flies. Here, analysis of the bacterial composition of the Drosophila gut by next-generation sequencing revealed that gut microbiota comprising one dominant genus of Acetobacter in non-TG-RNAi flies was shifted to that comprising two dominant genera of Acetobacter and Providencia in TG-RNAi flies. Four bacterial strains, including Acetobacter persici SK1 and Acetobacter indonesiensis SK2, Lactobacillus pentosus SK3, and Providencia rettgeri SK4, were isolated from the midgut of TG-RNAi flies. SK1 exhibited the highest resistance to the IMD-AMPs Cecropin A1 and Diptericin among the isolated bacteria. In contrast, SK4 exhibited considerably lower resistance against Cecropin A1, whereas SK4 exhibited high resistance to hypochlorous acid. The resistance of strains SK1-4 against IMD-AMPs in in vitro assays could not explain the shift of the microbiota in the gut of TGRNAi flies. The lifespan was reduced in gnotobiotic flies that ingested both SK4 and SK1, concomitant with the production of reactive oxygen species and apoptosis in the midgut, whereas the survival rate was not altered in gnotobiotic flies that monoingested either SK4 or SK1. Interestingly, significant amounts of reactive oxygen species were detected in the midgut of gnotobiotic flies that ingested SK4 and SK2, concomitant with no significant apoptosis in the midgut. In gnotobiotic flies that co-ingested SK4 and SK1, an additional unknown factor(s) may be required to cause midgut apoptosis.Foreign substances, including foods, minerals, and microbes, continually pass through the intestinal tract and attach to the gut epithelium. Development of physical and immunologic barriers against foreign substances is thus essential to protect the gut epithelia. Healthy and balanced gut microbiota provide essential nutrients for their host and help to maintain gut immune homeostasis, whereas disruption of the balance, called dysbiosis, is associated with various animal diseases (1, 2). The fruit fly, Drosophila melanogaster, is a useful model for investigating the close relationship between bacteria and bacteria or host and bacteria interactions (3, 4), and the gut microbial community of Drosophila comprises ϳ10 5 microbes of ϳ20 species (5-7). The Drosophila gut is functionally analogous to the mammalian intestinal tract (8, 9), producing antimicrobial peptides (AMPs) 2 and reactive oxygen species (ROS) (10, 11). Microbes or microbe-derived immune elicitors in the fly gut can initiate several immune signaling pathways, such as the immune deficiency (IMD) pathway activated by peptidoglycans to produce AMPs and the dual oxidase (DUOX) signaling pathway activated by uracils to produce . In addition to pathogenic bacteria, commensal microbe-derived peptidoglycans constitutively acti...

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Host Species and Environmental Effects on Bacterial Communities Associated with Drosophila in the Laboratory and in the Natural Environment

Cited by 223 publications

References 58 publications

Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype

The Host as the Driver of the Microbiota in the Gut and External Environment of Drosophila melanogaster

RNA Interference Directed against the Transglutaminase Gene Triggers Dysbiosis of Gut Microbiota in Drosophila

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