Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota

Rawls, John F.; Samuel, Buck S.; Gordon, Jeffrey I.

doi:10.1073/pnas.0400706101

Cited by 836 publications

(826 citation statements)

References 64 publications

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“…Vast numbers of microbes are present in the animal gastrointestinal (GI) tract and are critical for the nutrition and health of the host (Bäckhed et al, 2004;Gordon, 2005). The physiological role of microbiota in fish guts has been extensively studied (Rawls et al, 2004(Rawls et al, , 2007Bates et al, 2006). The intestinal microflora of fish, primarily established at the yolk sac stage when ingestion of bacteria in ambient water starts (Hansen and Olafsen, 1999), are important for immune tolerance and for the successful rearing of several freshwater fish species in early life stages (Sugita et al, 1994).…”

Section: Introductionmentioning

confidence: 99%

Host species as a strong determinant of the intestinal microbiota of fish larvae

et al. 2012

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We investigated the influence of host species on intestinal microbiota by comparing the gut bacterial community structure of four cohabitating freshwater fish larvae, silver carp, grass carp, bighead carp, and blunt snout bream, using denaturing gradient gel electrophoresis (DGGE) of the amplified 16S and 18S rRNA genes. Similarity clustering indicated that the intestinal microbiota derived from these four fish species could be divided into four groups based on 16S rRNA gene similarity, whereas the eukaryotic 18S rRNA genes showed no distinct groups. The water sample from the shared environment contained microbiota of an independent group as indicated by both 16S and 18S rRNA genes segments. The bacterial community structures were visualized using rank-abundance plots fitted with linear regression models. Results showed that the intestinal bacterial evenness was significantly different between species (P<0.05) and between species and the water sample (P<0.01). Thirty-five relatively dominant bands in DGGE patterns were sequenced and grouped into five major taxa: Proteobacteria (26), Actinobacteria (5), Bacteroidetes (1), Firmicutes (2), and Cyanobacterial (1). Six eukaryotes were detected by sequencing 18S rRNA genes segments. The present study suggests that the intestines of the four fish larvae, although reared in the same environment, contained distinct bacterial populations, while intestinal eukaryotic microorganisms were almost identical.

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Section: Introductionmentioning

confidence: 99%

Host species as a strong determinant of the intestinal microbiota of fish larvae

et al. 2012

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“…In some cases, extensive genetic coevolution between the animal host and microbes has resulted in obligate, highly specific, nutritional symbioses involving one or a few vertically transmitted microbial species, such as the endosymbionts of some hydrothermal vent invertebrates and those of plant sap-feeding insects (Moran, 2007;Dubilier et al, 2008). Even for more complex animal gut microbial communities, acquired and maintained dynamically after hatching or birth, there are likely host-microbe specificity determinants, as revealed by natural colonization and experimental microbiota transplantation across host species (Rawls et al, 2004;Rawls et al, 2006;Palmer et al, 2007;Morowitz et al, 2011). Distinct community structure and composition characterizes different vertebrate and invertebrate species in their natural environments, global microbiota and interspecies relatedness, reflecting host phylogeny and incorporating elements of developmental and nutritional specialization (Ley et al, 2008a, b;Ochman et al, 2010;Yidirim et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Host genetic and environmental effects on mouse intestinal microbiota

et al. 2012

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The mammalian gut harbors complex and variable microbial communities, across both host phylogenetic space and conspecific individuals. A synergy of host genetic and environmental factors shape these communities and account for their variability, but their individual contributions and the selective pressures involved are still not well understood. We employed barcoded pyrosequencing of V1-2 and V4 regions of bacterial small subunit ribosomal RNA genes to characterize the effects of host genetics and environment on cecum assemblages in 10 genetically distinct, inbred mouse strains. Eight of these strains are the foundation of the Collaborative Cross (CC), a panel of mice derived from a genetically diverse set of inbred founder strains, designed specifically for complex trait analysis. Diversity of gut microbiota was characterized by complementing phylogenetic and distance-based, sequence-clustering approaches. Significant correlations were found between the mouse strains and their gut microbiota, reflected by distinct bacterial communities. Cohabitation and litter had a reduced, although detectable effect, and the microbiota response to these factors varied by strain. We identified bacterial phylotypes that appear to be discriminative and strainspecific to each mouse line used. Cohabitation of different strains of mice revealed an interaction of host genetic and environmental factors in shaping gut bacterial consortia, in which bacterial communities became more similar but retained strain specificity. This study provides a baseline analysis of intestinal bacterial communities in the eight CC progenitor strains and will be linked to integrated host genotype, phenotype and microbiota research on the resulting CC panel.

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“…We have developed gnotobiotic husbandry methods for the zebrafish, and used them to reveal host responses to the gut microbiota including effects on innate immunity, nutrient metabolism, and intestinal epithelial differentiation and renewal (Rawls et al, 2004(Rawls et al, , 2006Bates et al, 2006Bates et al, , 2007Cheesman and Guillemin, 2007;Cheesman et al, 2011;Kanther and Rawls, 2010). Preliminary insights into the membership of the zebrafish gut microbiota have been provided by sequencing libraries of bacterial 16S rRNA genes amplified from pooled intestinal samples from zebrafish reared in laboratory aquaculture facilities (Rawls et al, 2004(Rawls et al, , 2006Bates et al, 2006;Brugman et al, 2009). These results indicate that the zebrafish gut microbiota is numerically dominated at all stages of the zebrafish life cycle by members of the bacterial phylum Proteobacteria, with the phyla Firmicutes and Fusobacteria also prevalent during larval and adult stages respectively.…”

Section: Introductionmentioning

confidence: 99%

Evidence for a core gut microbiota in the zebrafish

et al. 2011

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Experimental analysis of gut microbial communities and their interactions with vertebrate hosts is conducted predominantly in domesticated animals that have been maintained in laboratory facilities for many generations. These animal models are useful for studying coevolved relationships between host and microbiota only if the microbial communities that occur in animals in lab facilities are representative of those that occur in nature. We performed 16S rRNA gene sequence-based comparisons of gut bacterial communities in zebrafish collected recently from their natural habitat and those reared for generations in lab facilities in different geographic locations. Patterns of gut microbiota structure in domesticated zebrafish varied across different lab facilities in correlation with historical connections between those facilities. However, gut microbiota membership in domesticated and recently caught zebrafish was strikingly similar, with a shared core gut microbiota. The zebrafish intestinal habitat therefore selects for specific bacterial taxa despite radical differences in host provenance and domestication status.

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Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota

Abstract: Danio rerio ͉ symbiosis ͉ host-microbial cross-talk ͉ mice ͉ DNA microarrays

Cited by 836 publications

References 64 publications

Host species as a strong determinant of the intestinal microbiota of fish larvae

Host species as a strong determinant of the intestinal microbiota of fish larvae

Host genetic and environmental effects on mouse intestinal microbiota

Evidence for a core gut microbiota in the zebrafish

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