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

Michael P. Doane, Megan M. Morris, Bhavya Papudeshi, Lauren Allen, Dnyanada Pande, John M. Haggerty, Shaili Johri, Abigail C. Turnlund, Meredith Peterson, Dovi Kacev, Andy Nosal, Deni Ramirez, Kevin Hovel, Julia Ledbetter, Amanda Alker, Jackeline Avalos, Kristi Baker, Shruti Bhide, Emma Billings, Steven ByrumMolly Clemens, Amelia Juliette Demery, Lais Farias Oliveira Lima, Oscar Gomez, Omar Gutierrez, Selena Hinton, Donald Kieu, Angie Kim, Rebeca Loaiza, Alexander Martinez, Jordan McGhee, Kristine Nguyen, Sabrina Parlan, Amanda Pham, Rosalyn Price-Waldman, Robert A. Edwards, Elizabeth A. Dinsdale

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish
Article number93
Number of pages15
JournalMicrobiome
Volume8
DOIs
Publication statusPublished - 13 Jun 2020
Externally publishedYes

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© The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
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Keywords

  • Community ecology
  • Elasmobranch skin
  • Metagenomics
  • Microbial community
  • Microbiome
  • Phylosymbiosis
  • Teleost
  • Vertebrate fishes

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