Dataset Information

The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge.

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. Video abstract.

SUBMITTER: Doane MP

PROVIDER: S-EPMC7293782 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge.

Doane Michael P MP Morris Megan M MM Papudeshi Bhavya B Allen Lauren L Pande Dnyanada D Haggerty John M JM Johri Shaili S Turnlund Abigail C AC Peterson Meredith M Kacev Dovi D Nosal Andy A Ramirez Deni D Hovel Kevin K Ledbetter Julia J Alker Amanda A Avalos Jackeline J Baker Kristi K Bhide Shruti S Billings Emma E Byrum Steven S Clemens Molly M Demery Amelia Juliette AJ Lima Lais Farias Oliveira LFO Gomez Oscar O Gutierrez Omar O Hinton Selena S Kieu Donald D Kim Angie A Loaiza Rebeca R Martinez Alexander A McGhee Jordan J Nguyen Kristine K Parlan Sabrina S Pham Amanda A Price-Waldman Rosalyn R Edwards Robert A RA Dinsdale Elizabeth A EA

Microbiome 20200613 1

<h4>Background</h4>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 am ...[more]

PMID: 32534596

Similar Datasets

Project description:Recent advances in carbohydrate chemistry, chemical biology, and mass spectrometric techniques have opened the door to rapid progress in uncovering the function and diversity of glycan structures associated with human health and disease. These strategies can be equally well applied to advance non-human health care research. To date, the glycomes of only a handful of non-human, non-domesticated vertebrates have been analyzed in depth due to the logistic complications associated with obtaining or handling wild-caught or farm-raised specimens. In contrast, the last 2 decades have seen advances in proteomics, glycoproteomics, and glycomics that have significantly advanced efforts to identify human serum/plasma biomarkers for various diseases. In this study, we investigated N-glycan structural diversity in serum harvested from five cultured fish species. This biofluid is a useful starting point for glycomic analysis because it is rich in glycoproteins, can be acquired in a sustainable fashion, and its contents reflect dynamic physiologic changes in the organism. Sera acquired from two chondrostrean fish species, the Atlantic sturgeon and shortnose sturgeon, and three teleost fish species, the Atlantic salmon, Arctic char, and channel catfish, were delipidated by organic extraction and the resulting protein-rich preparations sequentially treated with trypsin and PNGaseF to generate released N-glycans for structural analysis. Released N-glycans were analyzed as their native or permethylated forms by nanospray ionization mass spectrometry in negative or positive mode. While the basic biosynthetic pathway that initiates the production of glycoprotein glycan core structures is well-conserved across the teleost fish species examined in this study, species-specific structural differences were detected across the five organisms in terms of their monosaccharide composition, sialylation pattern, fucosylation, and degree of O-acetylation. Our methods and results provide new contributions to a growing library of datasets describing fish N-glycomes that can eventually establish species-normative baselines for assessing N-glycosylation dynamics associated with pathogen invasion, environmental stress, and fish immunologic responses.

Dataset Information

The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge.

Background

Results

Conclusion

Publications

The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets