The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge
Open Access
- 13 June 2020
- journal article
- research article
- Published by Springer Science and Business Media LLC in Microbiome
- Vol. 8 (1), 1-15
- https://doi.org/10.1186/s40168-020-00840-x
Abstract
Background The vertebrate clade diverged into Chondrichthyes (sharks, rays, and chimeras) and Osteichthyes fishes (bony fishes) approximately 420 mya, with each group accumulating vast anatomical and physiological differences, including skin properties. The skin of Chondrichthyes fishes is covered in dermal denticles, whereas Osteichthyes fishes are covered in scales and are mucous rich. The divergence time among these two fish groups is hypothesized to result in predictable variation among symbionts. Here, using shotgun metagenomics, we test if patterns of diversity in the skin surface microbiome across the two fish clades match predictions made by phylosymbiosis theory. We hypothesize (1) the skin microbiome will be host and clade-specific, (2) evolutionary difference in elasmobranch and teleost will correspond with a concomitant increase in host-microbiome dissimilarity, and (3) the skin structure of the two groups will affect the taxonomic and functional composition of the microbiomes. Results We show that the taxonomic and functional composition of the microbiomes is host-specific. Teleost fish had lower average microbiome within clade similarity compared to among clade comparison, but their composition is not different among clade in a null based model. Elasmobranch's average similarity within clade was not different than across clade and not different in a null based model of comparison. In the comparison of host distance with microbiome distance, we found that the taxonomic composition of the microbiome was related to host distance for the elasmobranchs, but not the teleost fishes. In comparison, the gene function composition was not related to the host-organism distance for elasmobranchs but was negatively correlated with host distance for teleost fishes. Conclusion Our results show the patterns of phylosymbiosis are not consistent across both fish clades, with the elasmobranchs showing phylosymbiosis, while the teleost fish are not. The discrepancy may be linked to alternative processes underpinning microbiome assemblage, including possible historical host-microbiome evolution of the elasmobranchs and convergent evolution in the teleost which filter specific microbial groups. Our comparison of the microbiomes among fishes represents an investigation into the microbial relationships of the oldest divergence of extant vertebrate hosts and reveals that microbial relationships are not consistent across evolutionary timescales.Funding Information
- National Science Foundation (1323809, 1330800)
This publication has 64 references indexed in Scilit:
- Microbes, metagenomes and marine mammals: enabling the next generation of scientist to enter the genomic eraBMC Genomics, 2013
- Basics of skin structure and function in elasmobranchs: a reviewJournal of Fish Biology, 2012
- A Format for Phylogenetic PlacementsPLOS ONE, 2012
- Comparative analysis of innate immune parameters of the skin mucous secretions from certain freshwater teleosts, inhabiting different ecological nichesFish Physiology and Biochemistry, 2012
- The Phylogenetic Kantorovich–Rubinstein Metric for Environmental Sequence SamplesJournal of the Royal Statistical Society Series B: Statistical Methodology, 2012
- RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing dataBioinformatics, 2011
- Bacterial community assembly based on functional genes rather than speciesProceedings of the National Academy of Sciences of the United States of America, 2011
- Quality control and preprocessing of metagenomic datasetsBioinformatics, 2011
- From Structure to Function: the Ecology of Host-Associated Microbial CommunitiesMicrobiology and Molecular Biology Reviews, 2010
- Myxinidin, A Novel Antimicrobial Peptide from the Epidermal Mucus of Hagfish, Myxine glutinosa L.Marine Biotechnology, 2009