Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis

Abstract

Symbiotic bacteria often help their hosts acquire nutrients from their diet, showing trends of co-evolution and independent acquisition by hosts from the same trophic levels. While these trends hint at important roles for biotic factors, the effects of the abiotic environment on symbiotic community composition remain comparably understudied. In this investigation, we examined the influence of abiotic and biotic factors on the gut bacterial communities of fish from different taxa, trophic levels and habitats. Phylogenetic and statistical analyses of 25 16S rRNA libraries revealed that salinity, trophic level and possibly host phylogeny shape the composition of fish gut bacteria. When analysed alongside bacterial communities from other environments, fish gut communities typically clustered with gut communities from mammals and insects. Similar consideration of individual phylotypes (vs. communities) revealed evolutionary ties between fish gut microbes and symbionts of animals, as many of the bacteria from the guts of herbivorous fish were closely related to those from mammals. Our results indicate that fish harbour more specialized gut communities than previously recognized. They also highlight a trend of convergent acquisition of similar bacterial communities by fish and mammals, raising the possibility that fish were the first to evolve symbioses resembling those found among extant gut fermenting mammals.

Fig. 1

(A) Bacterial species from 25 fish gut communities classified into the phylum level. Bar graphs for each library represent the percentage of species assigned to each phylum with ≥80% bootstrap confidence. Names of the fish hosts are listed along the horizontal axis. To differentiate between libraries of the same species, the authors of the relevant studies are listed in parentheses, while ‘CI’ indicates the sequences culture independently derived from the Kim et al. (2007) Oncorhynchus mykiss samples. The D. rerio libraries from the Roeselers et al. (2011) study are differentiated by location name in parentheses. (B) Bacterial OTUs from 25 fish gut communities classified to the order level. Bar graphs for each library represent the percentage of species assigned to each order with ≥80% bootstrap confidence.

Fig. 2

Results of principal coordinates analysis based on pairwise unweighted UniFrac distances. Symbols representing individual communities are coloured by trophic level (green: herbivores, red: carnivores and yellow: omnivores). Shapes represent the habitats from which the samples were derived (circle: saltwater, triangle: estuarine, square: freshwater, diamond: migratory fish species between fresh and saltwater, all of which were sampled from freshwater). Open symbols represent cultured bacterial communities, while solid symbols represent communities studied through culture-independent means. Symbols with ‘D’ on the top left illustrate individual zebrafish libraries, while those with ‘O’ represent rainbow trout libraries.

Fig. 3

(A) Principal coordinates analysis (PCoA) analysis illustrating similarity of bacterial communities from fish guts and other communities (Axes 1 and 2) across trophic levels and sampling methodologies. Fish are distributed among other bacterial communities, but they cluster with each other along trophic levels. (B) PCoA analysis illustrating similarity of bacterial communities from fish guts and other communities (Axes 1 and 3) based on habitat salinity. In this figure, PCoA 3 is shown because the difference in habitat salinity separates along this axis. The fish from estuarine habitats appear to be more similar to fish from freshwater, but the environmental communities from mixed salinity habitats cluster more with saltwater bacterial communities.

Fig. 4

Lifestyles of bacteria related to fish gut microbes. After constructing a phylogeny with 16S rRNA sequences from bacteria of fish guts and their top BLASTn hits, all representative sequences (one per 97% OTU) were categorized based on their relatedness to microbes from vertebrate guts, other animals (or vertebrate tissues), plants and both natural environmental and artificial habitats. The percentage of species (i.e. 97% OTUs) from each library falling into one of the 14 designated categories (see Table 3 for classification criteria) is illustrated using colour-coded bar graphs. For further clarity, trophic level and habitat type for studied fish hosts are indicated to the left of the Y-axis (herbivorous fish are highlighted at the bottom of the graph), while general groups of bacterial lifestyles are revealed to the right of the category legend. ‘M‘ symbols after host species names indicate that these species are known to migrate between fresh and saltwater. Note that herbivores show enrichment for microbes from categories 1 and 2, indicating that they are closely related to gut associates of other vertebrates—mostly mammals.