Identifying strains that contribute to complex diseases through the study of microbial inheritance

Faith, Jeremiah J.; Colombel, Jean-Frédééric; Gordon, Jeffrey I.

doi:10.1073/pnas.1418781112

Cited by 67 publications

(60 citation statements)

References 80 publications

(79 reference statements)

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“…This study on the relationship between Drosophila and its gut microbiota demonstrates that relatively nonspecific associations that apparently lack sophisticated behavioral mechanisms for controls over the microbiota can similarly play a role in shaping microbiota communities in the wider environment. Priorities for future research include quantitative analysis of the dynamics of bacterial transfer between the host and external environment (45) and investigation of how the principles of these interactions, identified under defined conditions on standardized food substrates, apply to the spatiotemporally complex habitat of a rotting fruit under natural conditions.…”

Section: Discussionmentioning

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

117

119

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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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Section: Discussionmentioning

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

117

119

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“…Infants are born near sterile and continually acquire microbial colonists until reaching an adult-like state at around 2-3 yr of age (Cilieborg et al 2012;Faith et al 2015). The microbiota during the first 100 d of life is especially important, as dysbiosis during this "critical window" has been linked to a number of problems later in life, especially relating to the developing immune system (Costello et al 2012;Cahenzli et al 2013;Sim et al 2013;Arrieta et al 2015).…”

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confidence: 99%

Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates

et al. 2017

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The initial microbiome impacts the health and future development of premature infants. Methodological limitations have led to gaps in our understanding of the habitat range and subpopulation complexity of founding strains, as well as how different body sites support microbial growth. Here, we used metagenomics to reconstruct genomes of strains that colonized the skin, mouth, and gut of two hospitalized premature infants during the first month of life. Seven bacterial populations, considered to be identical given whole-genome average nucleotide identity of >99.9%, colonized multiple body sites, yet none were shared between infants. Gut-associated Citrobacter koseri genomes harbored 47 polymorphic sites that we used to define 10 subpopulations, one of which appeared in the gut after 1 wk but did not spread to other body sites. Differential genome coverage was used to measure bacterial population replication rates in situ. In all cases where the same bacterial population was detected in multiple body sites, replication rates were faster in mouth and skin compared to the gut. The ability of identical strains to colonize multiple body sites underscores the habit flexibility of initial colonists, whereas differences in microbial replication rates between body sites suggest differences in host control and/or resource availability. Population genomic analyses revealed microdiversity within bacterial populations, implying initial inoculation by multiple individual cells with distinct genotypes. Overall, however, the overlap of strains across body sites implies that the premature infant microbiome can exhibit very low microbial diversity.

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“…In addition, host genetics, surrounding conditions, and antibiotic treatment are involved in the formation and modulation of intestinal microbiota [49][50][51]. After introducing solid foods, the infants' intestinal microbiota undergo a rapid diversification and shift toward an adult-like microbiota, which will resemble that of an adult by 3 years old [52]. Once established, the gut microbiota tend to be relatively stable via subsequent regeneration itself after the temporary disruption of diet changes such as short-term travels and antibiotic use, al- though high variability between individuals is observed.…”

Section: Initial Colonization and Immune-mediated Diseasesmentioning

confidence: 99%

The Local Defender and Functional Mediator: Gut Microbiome

Yang¹,

Duan²

2018

Digestion

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Background: The gut microbiome has been developing and making adaption all the time, which is consistent with their host from the initial colonization at birth or earlier. Emerging evidence is showing that dysbiosis is involved in various diseases associated with immune, metabolism, infection, nervous system, social behaviors, and psychopathology, etc., maybe via modulating gut barrier, microbiome-gut-brain axis, or some metabolites like short-chain fatty acids (SCFAs). Summary: In the review, we will conclude the recent researches related to the influence of microbiome on local structure, function, regulation, metabolism of gut, and systematic modulation to the host, as well as some affective factors such as diet or antibiotics. Key Messages: It is a reasonable hypothesis that the balance of bioactive factors or cells and the opposites such as the regulatory T/helper T17 balance and interleukin (IL)-10/IL-17 balance plays a vital role in homeostasis of immunity system. Meanwhile, the link between gut microbiome and immune system via microbiota-derived metabolite SCFAs involved in multi-function of the host locally and systematically has been revealed. We hope to contribute to the microbiome-targeted treatment and prevention of some diseases.

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Identifying strains that contribute to complex diseases through the study of microbial inheritance

Cited by 67 publications

References 80 publications

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

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

Identical bacterial populations colonize premature infant gut, skin, and oral microbiomes and exhibit different in situ growth rates

The Local Defender and Functional Mediator: Gut Microbiome

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