TY - JOUR
T1 - The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge
AU - Doane, Michael P.
AU - Morris, Megan M.
AU - Papudeshi, Bhavya
AU - Allen, Lauren
AU - Pande, Dnyanada
AU - Haggerty, John M.
AU - Johri, Shaili
AU - Turnlund, Abigail C.
AU - Peterson, Meredith
AU - Kacev, Dovi
AU - Nosal, Andy
AU - Ramirez, Deni
AU - Hovel, Kevin
AU - Ledbetter, Julia
AU - Alker, Amanda
AU - Avalos, Jackeline
AU - Baker, Kristi
AU - Bhide, Shruti
AU - Billings, Emma
AU - Byrum, Steven
AU - Clemens, Molly
AU - Demery, Amelia Juliette
AU - Lima, Lais Farias Oliveira
AU - Gomez, Oscar
AU - Gutierrez, Omar
AU - Hinton, Selena
AU - Kieu, Donald
AU - Kim, Angie
AU - Loaiza, Rebeca
AU - Martinez, Alexander
AU - McGhee, Jordan
AU - Nguyen, Kristine
AU - Parlan, Sabrina
AU - Pham, Amanda
AU - Price-Waldman, Rosalyn
AU - Edwards, Robert A.
AU - Dinsdale, Elizabeth A.
N1 - Copyright the Author(s) 2020. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.
PY - 2020/6/13
Y1 - 2020/6/13
N2 - 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. [MediaObject not available: see fulltext.].
AB - 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. [MediaObject not available: see fulltext.].
KW - Community ecology
KW - Elasmobranch skin
KW - Metagenomics
KW - Microbial community
KW - Microbiome
KW - Phylosymbiosis
KW - Teleost
KW - Vertebrate fishes
UR - http://www.scopus.com/inward/record.url?scp=85086620356&partnerID=8YFLogxK
U2 - 10.1186/s40168-020-00840-x
DO - 10.1186/s40168-020-00840-x
M3 - Article
C2 - 32534596
AN - SCOPUS:85086620356
VL - 8
SP - 1
EP - 15
JO - Microbiome
JF - Microbiome
SN - 2049-2618
IS - 1
M1 - 93
ER -