Fish gill mucus is a bacterial oasis in tropical seas

Bacteria form symbioses with a range of eukaryotic hosts, including humans and a vast array of marine invertebrates. Coral bacterial symbionts have received particular attention, while fish microbiomes have been comparatively less studied; however, this is now changing due to recent efforts to characterise the “fish gastrointestinal microbiome”, with a focus on commercially important species and the hope to increase their health and nutritional status by targeting their microbial symbionts (Tarnecki et al., 2017). Moreover, a number of studies have been published on other less exploited fish species. For instance, Miriam Reverter and her colleagues recently described the abundance and diversity of bacteria associated with the gill mucus in four butterflyfish species, drawing insightful links with the ecology of their animal hosts (Reverter et al., 2017). In the mentioned study, the V1-V3 16S rDNA barcodes were sequenced from 4 sympatric butterflyfish species (Chaetodon lunulatus, C. ornatissimus, C. vagabundus and C. reticulatus) in order to identify their gill mucus-associated bacteria. The sequences were quality checked and diversity was estimated with a range of indices from a rarefied OTU table.

The “core microbiome”, i.e. bacteria found in all four species of fish, comprised only 26 OTUs (~ 2.5% of the total OTUs) belonging to the Proteobacteria, Firmicutes and Actinobacteria, with an additional Cyanobacteria OTU. The former three phyla were also the most abundant in terms of OTUs, though the authors were rightly cautious by recognising that OTU and cellular abundances do not always coincide. C. lunulatus was shown to have the highest abundance of unique OTUs, and the authors related this finding to the absence of monogean parasitic flatworms in this fish species; however, the study did not assess the presence of the said parasites on the remaining fish species.

The phyla identified as the most abundant in the four butterflyfishes’ gill mucus also dominated gastrointestinal microbiomes of most other fishes studied to date (Tarnecki et al., 2017). In light of this, the authors acknowledged the often-seen correlation between microbiome composition and diet, and the study offers further support for this: in fact, C. lunulatus and C. ornatissimus, both corallivores, had the most taxonomically similar gill mucus-associated bacterial assemblage. The two species are also the least phylogenetically distant, therefore the authors propose phylogeny as another possible factor influencing the composition of their bacterial microbiomes, though it is unclear how this might result. Arguably, diet and host ecology would be expected to play a more significant role in sympatric close relatives, such as the four chaetodontids under investigation. At the family level, there was a relatively high abundance of Vibrionaceae in C. lunulatus and C. ornatissimus, and Rhodobacteraceae in C. reticulatus and C. vagabundus. Representatives from both bacterial families are known and potential coral pathogens respectively (Sunagawa et al., 2009), and, considering the opportunistic nature of many coral pathogens (Rohwer & Youle, 2010), it would be interesting to assess the composition changes of the two groups in diseased butterflyfish.

Perhaps most remarkably, the diversity and abundance of bacterial symbionts associated with fish gill mucus were comparable to coral-associated bacterial communities. The hypothesis made by the authors, that fish mucus represents a “reservoir for coral reef bacterial diversity”, awaits further investigation, as does the role of host phylogeny in shaping symbiotic bacterial communities. Future experiments aiming to determine the mode of host “colonisation” used by bacteria, and encompassing a more evolutionary distant set of host species might help answer these questions and improve our understanding of bacterial symbionts of marine fishes.

Reviewed article:

Reverter, M., Sasal, P., Tapissier-Bontemps, N., Lecchini, D. & Suzuki, M. (2017) 'Characterisation of the gill mucosal bacterial communities of four butterflyfish species: a reservoir of bacterial diversity in coral reef ecosystems'. FEMS Microbiol Ecol, 93 (6).

References

Rohwer, F. & Youle, M. (2010) 'Coral Diseases', Coral Reefs in the Microbial Seas. Plaid Press.

Sunagawa, S., DeSantis, T. Z., Piceno, Y. M., Brodie, E. L., DeSalvo, M. K., Voolstra, C. R., Weil, E., Andersen, G. L. & Medina, M. (2009) 'Bacterial diversity and White Plague Disease-associated community changes in the Caribbean coral Montastraea faveolata'. ISME J, 3 (5), pp. 512-521.

Tarnecki, A. M., Burgos, F. A., Ray, C. L. & Arias, C. R. (2017) 'Fish intestinal microbiome: diversity and symbiosis unravelled by metagenomics'. Journal of Applied Microbiology, 123 (1), pp. 2-17.