The ‘Inner Fish’: How Lifestyle Shapes Fish Gut Bacteria and some Surprising Similarities to Mammalian Gut Microbiota

Bacterial community composition is known to be heavily influenced by the properties of the external environment.  Correspondingly, the host environment itself may be heavily influenced by the presence of particular bacteria, as with metazoans inhabited by bacterial endosymbionts. An especially important example of such bacterial function is observed in vertebrate gut microbiota, whose critical physiological roles include complex carbohydrate digestion and lipid storage regulation.  Although the range of environmental, ecological and physiological factors which shape vertebrate microbiota have been well reported in mammals (where similar gut communities have been found in taxa with high phylogenetic relatedness or similar diets), the importance of these factors in the ancient and highly diverse group of aquatic vertebrates generally referred to as ‘fish’, is comparatively understudied.

Sullam et al. (2012) performed a meta-analysis investigating the taxonomic and phylogenetic similarity of fish gut bacteria from teleost hosts of different habitats, trophic levels and taxa.  The authors accomplished this using 16S rRNA gene sequence data from 17 different bacterial fish-gut community data sets (‘libraries’), including data for the gut bacteria of the Trinidadian guppy, Poecilia reticulata, generated by the authors.  The fish gut communities were also compared to those of other vertebrate hosts, non-vertebrate eukaryotes, and free-living habitats.  Statistical tests and phylogenetic analyses were carried out on 1054 operational taxonomic units (OTUs), each a representative of OTUs that were grouped by ≥97% similarity in 16S rDNA sequences.

Across all fish gut libraries, Proteobacteria were found to be the dominant phyla (mean: 62.51%), but when representative OTUs were classified by order, marine and freshwater (FW) derived communities were found to vary significantly.  FW hosts harboured a greater proportion of Aeromonadales and Enterobacteriales, whereas Marine communities had a greater proportion of Vibrionales.  Distinct differences were observed also over fish trophic levels.  Compared to carnivorous of omnivorous fish-gut communities, herbivorous fish communities had a greater number of Clostridiales, Bacteroidales and Verrucomicrobiales, but less Desulfovibrionales and Aeromonadales.  Omnivorous fish harboured a greater proportion of Rhizobiales, Fusobacteriales and Planctomycetales then the other trophic groups. 

Analysis of a phylogeny created by the authors was performed via Principle Coordinate Analysis (PCoA).  This revealed clustering due to habitat salinity, trophic level and method of sampling (i.e. culture dependent vs. culture independent), but whether the fish were from a natural environment or reared (i.e. via aquaculture or in a lab) was not shown to significantly affect microbial diversity.  The results of PCoA between fish-gut communities and other free-living and host-associated bacterial communities revealed some interesting insights into fish-gut microbiota.  Most fish-gut communities from herbivorous and carnivorous fish clustered with those from herbivorous- and carnivorous-mammalian guts (respectively), whereas omnivorous fish communities all clustered near free-living ⁄ invertebrate-associated communities. 

It is particularly intriguing that in 3 of the 4 herbivorous fish-gut communities analysed, most of the representative OTUs belonged to lineages previously recorded in the guts of birds and mammals.  The authors suggest that these fish-gut communities may function in a similar fashion to those of mammalian herbivores, with gut fermentation being of major importance in both groups.  Sullam et al. (2012) go on to speculate that fish may have been the earliest vertebrate hosts of many such microbes, whose descendants continue to thrive in the mammalian gut during the present day.  More thorough sampling across fish groups is suggested in order to rule out convergent evolution of separate free-living lineages in similar gut environments (resulting in analogous, but phylogeneticly distinct gut communities).

Although the results of this meta-analysis are fascinating, the authors highlight the comparatively narrow range of hosts (in terms of phylogeny, ecology and trophic niche) whose gut microbiota could be analysed.  It would be fascinating to compare the microbial communities of elasmobranches or deep sea fish with the data explored in this report.  Sullam et al. (2012) also discuss the necessity of exploring the functional roles of fish microbes, and thus their potential to influence fish ecology and evolution (in which metagenomic analysis may be vital). 

It appears some fish-gut microbes may be as important to the ecology of certain fish, as those of the ruminant are vital to its continued existence.   I believe that in such a circumstance, it is apparent that bacteria have quite probability had a critical role of in the physiological evolution of these fish, and thus further investigation into this possibility is vital to our understanding of these fish species.

 

Sullam, Karen E, Steven D Essinger, Catherine a Lozupone, Michael P O’Connor, Gail L Rosen, Rob Knight, Susan S Kilham, and Jacob a Russell. 2012. “Environmental and Ecological Factors That Shape the Gut Bacterial Communities of Fish: a Meta-analysis.” Molecular Ecology 21: 3363–78.

http://www.ncbi.nlm.nih.gov/pubmed/22486918.