Microbiome in the Drosophila gut

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The microbiota describes the sum of all symbiotic microorganisms (mutualism, commensalism or pathogenic) living on or in an organism. The fruit fly Drosophila melanogaster is a model organism and known as one of the most investigated organisms worldwide. The microbiota in flies is less complex than that found in humans. It still has an influence on the fitness of the fly, [1] and it affects different life-history characteristics such as lifespan (life expectancy), resistance against pathogens (immunity) and metabolic processes (digestion). Considering the comprehensive toolkit available for research in Drosophila, analysis of its microbiome could enhance our understanding of similar processes in other types of host-microbiota interactions, including those involving humans. Microbiota plays key roles in the intestinal immune and metabolic responses via their fermentation product (short chain fatty acid), acetate. [2]

Contents

Microbial composition

Drosophila melanogaster possesses a comparatively simple gut microbiota, consisting of only few bacterial species, mainly from two bacterial taxonomic groups: Bacillota and Pseudomonadota. [3] [4] The most common species belong to the families Lactobacillaceae (abundance of approx. 30%, members of the Bacillota) and Acetobacteraceae (approx. 55%, members of the Proteobacteria). Other less common bacterial species are from the families Leuconostocaceae, Enterococceae, and Enterobacteriaceae (all with an abundance in between 2–4%). [4] The most common species include Lactobacillus plantarum , Lactobacillus brevis , Acetobacter pomorum and Enterococcus faecalis , while other species such as Acetobacter aceti , Acetobacter tropicalis and Acetobacter pasteurianus are also often found. [3]

The particular species of the host fly has a central influence on the composition and quality of the gut microbiota, even if flies are raised under similar conditions. [5] Nevertheless, the host's diet and nutritional environment also shape the exact composition of the microbiota. For instance the exact pH of the food can kill certain bacterial species. [3] In general, the type of food used by the fly affects the microbiota composition. [6] Mushroom feeder species like Drosophila fallen and MicroDrosophila sp. harbour many Lactobacillales and generally maintain high bacterial diversity in their guts. The microbiota of flower feeders such as Drosophila elegans and Drosophila flavohirta shows higher abundance of Enterobacteriaceae and to a lesser extent of acido-philic bacteria (such as Acetobacteraceae and Lactobacillaceae) if compared to fruit-eating species such as Drosophila hydei, Drosophila immigrans, Drosophila sulfurigaster, Drosophila melanogaster, Drosophila sechellia or Drosophila takahashii. [3] The microbial load and bacterial composition also vary with the age of the host fly. [3]

Microbiota transmission and establishment

Feeding is a key determinant of the microbiota composition. Not only the diet influences presence and abundance of the bacteria inside the gut, but the bacteria also need to be taken up continuously from the environment to prevail as members of the intestinal flora. [7] Feeding on feces seems to play a central role for establishment of the Drosophila microbiota, as it allows the flies to recycle the bacteria within a fly population at a particular time point and also across generations. Flies seed the embryonic eggshell with feces. Upon hatching, young larvae eat their eggshells and thereby pick up the bacteria. The microbiota, which subsequently establishes itself inside the gut of the developing larvae, is similar to that of the larvae's mothers. [8] This may further be promoted by the particular life history of the flies. Young adult flies, which harbor fewer bacteria than old flies, proliferate in an environment shaped by the feces of the preceding fly generation, thus allowing them to take up additional bacteria. [8]

Gut compartmentalization

In the gut of Drosophila melanogaster the composition and action of the microbiome appears to be tightly regulated within compartments, that is different sections of the intestines. This is indicated by the differential expression of genes, especially with a regulatory function, in the epithelium of different parts of the gut. In detail, the gut is compartmentalized into three parts, the foregut, the midgut, and the hindgut. While foregut and hindgut are lined with a cuticle formed by the ectodermal epithelium, the midgut is of endodermal origin. [9] In adult flies the midgut is further divided into five smaller regions. [10] The immune response varies among the gut regions. The immune deficiency (IMD) pathway responds to bacterial infections and is activated by certain receptors (e.g., the peptidoglycan receptor protein PGRP-LC). These receptors and also other components of the Drosophila immune system such as Toll receptor and dDUOX pathway molecules control immune responses in ectodermal tissue of the anterior gut. Moreover, the anterior midgut is enriched in certain antimicrobial peptides (AMPs). This suggests that the immune defence in this area is particularly responsive, possibly because this regions represents the first contact region for newly taken up food, microbiota, and/or intestinal pathogens. In the middle and posterior midgut, other genes such as the receptor PGRP-LB, which down-regulates the IMD immune response, are expressed, possibly in order to minimize expression of immune defence against the microbiota. In addition, the microbiota itself seems to control the expression of several Drosophila metabolic genes within the midgut, possibly to facilitate digestion of food. [11] Recently, IMD pathway in the anterior midgut region has been proposed to play multi-pronged roles to modulate key metabolic and mechanic functions in the gut. [12] Taken together, it appears that the interaction between host and microbiota is precisely regulated across different regions within the gut. [13]

Effects on behaviour

Drosophila microbiota have been implicated in mating success by influencing assortative mating; a phenomenon detected in some studies of Drosophila, [14] but not others. [15]

Effects on longevity

The microbiota seem to affect the lifespan of Drosophila melanogaster. To date, the mechanisms of this effect remain elusive.
Fruit flies raised under axenic conditions (i.e., without any bacteria in the environment) or cured of their microbiota with antibiotics had a shorter lifespan than flies raised under normal conditions. The microbiota influence on longevity seems to be particularly strong early in development. [16] To date, however, the exact mechanisms underlying these effects remain elusive. It is possible that the microbiota-induced proliferation of intestinal stem cells and associated metabolic homeostasis is important in this context. [17] In contrast, the microbiota seems to have a negative effect on lifespan in old Drosophila melanogaster, because their removal in ageing flies increases longevity. Old flies have a reduced ability to fight infections and this may also relate to the bacterial members of the microbiota. [18] In aged animals, immune responses may over-shoot, possibly harming the host and favoring colonization with pathogens (e.g. Gluconobacter morbifer). [19]

New method of microbiome analysis

Almost all current approaches for the characterization of Drosophila microbiota rely on destructive approaches, that is flies are killed, their gut is extracted and from these the bacteria are isolated and/or analyzed. For an assessment of microbiota dynamics across the lifespan of an individual fly or across development of a fly population, a non-destructive approach would be favorable. Such an approach was recently developed, focusing on the microbial characterization of fly feces. Fly feces are indeed informative on composition of the gut microbiota, since the diversity of gut bacteria, feces bacteria and bacteria of whole fly of Drosophila melanogaster are all strongly correlated. This new approach could be used to demonstrate the known influence of diets. [20]

Related Research Articles

<i>Drosophila melanogaster</i> Species of fruit fly

Drosophila melanogaster is a species of fly in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly" or "pomace fly". Starting with Charles W. Woodworth's 1901 proposal of the use of this species as a model organism, D. melanogaster continues to be widely used for biological research in genetics, physiology, microbial pathogenesis, and life history evolution. As of 2017, five Nobel Prizes have been awarded to drosophilists for their work using the insect.

<span class="mw-page-title-main">Human microbiome</span> Microorganisms in or on human skin and biofluids

The human microbiome is the aggregate of all microbiota that reside on or within human tissues and biofluids along with the corresponding anatomical sites in which they reside, including the skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, biliary tract, and gastrointestinal tract. Types of human microbiota include bacteria, archaea, fungi, protists and viruses. Though micro-animals can also live on the human body, they are typically excluded from this definition. In the context of genomics, the term human microbiome is sometimes used to refer to the collective genomes of resident microorganisms; however, the term human metagenome has the same meaning.

Acetobacter is a genus of acetic acid bacteria. Acetic acid bacteria are characterized by the ability to convert ethanol to acetic acid in the presence of oxygen. Of these, the genus Acetobacter is distinguished by the ability to oxidize lactate and acetate into carbon dioxide and water. Bacteria of the genus Acetobacter have been isolated from industrial vinegar fermentation processes and are frequently used as fermentation starter cultures.

Gnotobiosis refers to an engineered state of an organism in which all forms of life in or on it, including its microbiota, have been identified. The term gnotobiotic organism, or gnotobiote, can refer to a model organism that is colonized with a specific community of known microorganisms or that contains no microorganisms (germ-free) often for experimental purposes. The study of gnotobiosis and the generation of various types of gnotobiotic model organisms as tools for studying interactions between host organisms and microorganisms is referred to as gnotobiology.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gutmicrobiota are the microorganisms, including bacteria and archaea, that live in the digestive tracts of vertebrates including humans, and of insects. Alternative terms include gutflora and gutmicrobiome. The gastrointestinal metagenome is the aggregate of all the genomes of gut microbiota. In the human, the gut is the main location of human microbiota. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut-brain axis.

Dysbiosis is characterized by a disruption to the microbiome resulting in an imbalance in the microbiota, changes in their functional composition and metabolic activities, or a shift in their local distribution. For example, a part of the human microbiota such as the skin flora, gut flora, or vaginal flora, can become deranged, with normally dominating species underrepresented and normally outcompeted or contained species increasing to fill the void. Dysbiosis is most commonly reported as a condition in the gastrointestinal tract, particularly during small intestinal bacterial overgrowth (SIBO) or small intestinal fungal overgrowth (SIFO).

Methanobrevibacter smithii is the predominant archaeon in the microbiota of the human gut. M. smithii has a coccobacillus shape. It plays an important role in the efficient digestion of polysaccharides by consuming the end products of bacterial fermentation. Methanobrevibacter smithii is a single-celled microorganism from the Archaea domain. M. smithii is a methanogen, and a hydrogenotroph that recycles the hydrogen by combining it with carbon dioxide to methane. The removal of hydrogen by M. smithii is thought to allow an increase in the extraction of energy from nutrients by shifting bacterial fermentation to more oxidized end products.

<span class="mw-page-title-main">Microbial symbiosis and immunity</span>

Long-term close-knit interactions between symbiotic microbes and their host can alter host immune system responses to other microorganisms, including pathogens, and are required to maintain proper homeostasis. The immune system is a host defense system consisting of anatomical physical barriers as well as physiological and cellular responses, which protect the host against harmful microorganisms while limiting host responses to harmless symbionts. Humans are home to 1013 to 1014 bacteria, roughly equivalent to the number of human cells, and while these bacteria can be pathogenic to their host most of them are mutually beneficial to both the host and bacteria.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, symbiotic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

<span class="mw-page-title-main">Gut–brain axis</span> Biochemical signaling between the gastrointestinal tract and the central nervous system

The gut–brain axis is the two-way biochemical signaling that takes place between the gastrointestinal tract and the central nervous system (CNS). The term "gut–brain axis" is occasionally used to refer to the role of the gut microbiota in the interplay as well. The "microbiota–gut–brainaxis" explicitly includes the role of gut microbiota in the biochemical signaling events that take place between the GI tract and the CNS. Broadly defined, the gut–brain axis includes the central nervous system, neuroendocrine system, neuroimmune systems, the hypothalamic–pituitary–adrenal axis, sympathetic and parasympathetic arms of the autonomic nervous system, the enteric nervous system, vagus nerve, and the gut microbiota.

The altered Schaedler flora (ASF) is a community of eight bacterial species: two lactobacilli, one Bacteroides, one spiral bacterium of the Flexistipes genus, and four extremely oxygen sensitive (EOS) fusiform-shaped species. The bacteria are selected for their dominance and persistence in the normal microflora of mice, and for their ability to be isolated and grown in laboratory settings. Germ-free animals, mainly mice, are colonized with ASF for the purpose of studying the gastrointestinal (GI) tract. Intestinal mutualistic bacteria play an important role in affecting gene expression of the GI tract, immune responses, nutrient absorption, and pathogen resistance. The standardized microbial cocktail enabled the controlled study of microbe and host interactions, role of microbes, pathogen effects, and intestinal immunity and disease association, such as cancer, inflammatory bowel disease, diabetes, and other inflammatory or autoimmune diseases. Also, compared to germfree animals, ASF mice have fully developed immune system, resistance to opportunistic pathogens, and normal GI function and health, and are a great representation of normal mice.

<span class="mw-page-title-main">Pharmacomicrobiomics</span>

Pharmacomicrobiomics, first proposed by Prof. Marco Candela for the ERC-2009-StG project call and later publicly used in 2010, is defined as the effect of microbiome variations on drug disposition, action, and toxicity. Pharmacomicrobiomics is concerned with the interaction between xenobiotics, or foreign compounds, and the gut microbiome. It is estimated that over 100 trillion prokaryotes representing more than 1000 species reside in the gut. Within the gut, microbes help modulate developmental, immunological and nutrition host functions. The aggregate genome of microbes extends the metabolic capabilities of humans, allowing them to capture nutrients from diverse sources. Namely, through the secretion of enzymes that assist in the metabolism of chemicals foreign to the body, modification of liver and intestinal enzymes, and modulation of the expression of human metabolic genes, microbes can significantly impact the ingestion of xenobiotics.

<span class="mw-page-title-main">Human milk microbiome</span> Community of microorganisms in human milk

The human milk microbiota, also known as human milk probiotics (HMP), refers to the microbiota residing in the human mammary glands and breast milk. Human breast milk has been traditionally assumed to be sterile, but more recently both microbial culture and culture-independent techniques have confirmed that human milk contains diverse communities of bacteria which are distinct from other microbial communities inhabiting the human body.

<span class="mw-page-title-main">Drosocin</span> Antimicrobial peptide

Drosocin is a 19-residue long antimicrobial peptide (AMP) of flies first isolated in the fruit fly Drosophila melanogaster, and later shown to be conserved throughout the genus Drosophila. Drosocin is regulated by the NF-κB Imd signalling pathway in the fly.

<i>Drosophila quinaria</i> species group Species group of the subgenus Drosophila

The Drosophila quinaria species group is a speciose lineage of mushroom-feeding flies studied for their specialist ecology, their parasites, population genetics, and the evolution of immune systems. Quinaria species are part of the Drosophila subgenus.

<i>Drosophila innubila</i> Species of fly

Drosophila innubila is a species of vinegar fly restricted to high-elevation woodlands in the mountains of the southern USA and Mexico, which it likely colonized during the last glacial period. Drosophila innubila is a kind of mushroom-breeding Drosophila, and member of the Drosophila quinaria species group. Drosophila innubila is best known for its association with a strain of male-killing Wolbachia bacteria. These bacteria are parasitic, as they drain resources from the host and cause half the infected female's eggs to abort. However Wolbachia may offer benefits to the fly's fitness in certain circumstances. The D. innubila genome was sequenced in 2019.

<span class="mw-page-title-main">Imd pathway</span> Immune signaling pathway of insects

The Imd pathway is a broadly-conserved NF-κB immune signalling pathway of insects and some arthropods that regulates a potent antibacterial defence response. The pathway is named after the discovery of a mutation causing severe immune deficiency. The Imd pathway was first discovered in 1995 using Drosophila fruit flies by Bruno Lemaitre and colleagues, who also later discovered that the Drosophila Toll gene regulated defence against Gram-positive bacteria and fungi. Together the Toll and Imd pathways have formed a paradigm of insect immune signalling; as of September 2, 2019, these two landmark discovery papers have been cited collectively over 5000 times since publication on Google Scholar.

<span class="mw-page-title-main">Morganellaceae</span> Family of bacteria

The Morganellaceae are a family of Gram-negative bacteria that include some important human pathogens formerly classified as Enterobacteriaceae. This family is a member of the order Enterobacterales in the class Gammaproteobacteria of the phylum Pseudomonadota. Genera in this family include the type genus Morganella, along with Arsenophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia and Xenorhabdus.

<span class="mw-page-title-main">Bruno Lemaitre</span> French immunologist

Bruno Lemaitre is a French immunologist and a professor at the École Polytechnique Fédérale de Lausanne (EPFL). His research focuses on the mechanisms of innate immunity and endosymbiosis in Drosophila. Lemaitre has also authored several books on the topic of narcissism in science.

<i>Snodgrassella alvi</i> Species of bacterium

Snodgrassella alvi is a species of Gram-negative bacteria within the Neisseriaceae and the only known species of the genus Snodgrassella. It was isolated and scientifically described in 2012 by Waldan K. Kwong and Nancy A. Moran, who named the bacteria after the American entomologist Robert Evans Snodgrass.

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