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...
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| Format: | Article |
| Language: | English |
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BMC
2020-06-01
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| Series: | Microbiome |
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| Online Access: | http://link.springer.com/article/10.1186/s40168-020-00840-x |
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doaj-6f13b01e15184f108c5f0522c392e30c |
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| record_format |
Article |
| collection |
DOAJ |
| language |
English |
| format |
Article |
| sources |
DOAJ |
| author |
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 Byrum Molly 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 |
| spellingShingle |
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 Byrum Molly 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 The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge Microbiome Microbiome Phylosymbiosis Metagenomics Elasmobranch skin Teleost Vertebrate fishes |
| author_facet |
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 Byrum Molly 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 |
| author_sort |
Michael P. Doane |
| title |
The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge |
| title_short |
The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge |
| title_full |
The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge |
| title_fullStr |
The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge |
| title_full_unstemmed |
The skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge |
| title_sort |
skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes converge |
| publisher |
BMC |
| series |
Microbiome |
| issn |
2049-2618 |
| publishDate |
2020-06-01 |
| description |
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 |
| topic |
Microbiome Phylosymbiosis Metagenomics Elasmobranch skin Teleost Vertebrate fishes |
| url |
http://link.springer.com/article/10.1186/s40168-020-00840-x |
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| _version_ |
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doaj-6f13b01e15184f108c5f0522c392e30c2020-11-25T02:27:00ZengBMCMicrobiome2049-26182020-06-018111510.1186/s40168-020-00840-xThe skin microbiome of elasmobranchs follows phylosymbiosis, but in teleost fishes, the microbiomes convergeMichael P. Doane0Megan M. Morris1Bhavya Papudeshi2Lauren Allen3Dnyanada Pande4John M. Haggerty5Shaili Johri6Abigail C. Turnlund7Meredith Peterson8Dovi Kacev9Andy Nosal10Deni Ramirez11Kevin Hovel12Julia Ledbetter13Amanda Alker14Jackeline Avalos15Kristi Baker16Shruti Bhide17Emma Billings18Steven Byrum19Molly Clemens20Amelia Juliette Demery21Lais Farias Oliveira Lima22Oscar Gomez23Omar Gutierrez24Selena Hinton25Donald Kieu26Angie Kim27Rebeca Loaiza28Alexander Martinez29Jordan McGhee30Kristine Nguyen31Sabrina Parlan32Amanda Pham33Rosalyn Price-Waldman34Robert A. Edwards35Elizabeth A. Dinsdale36Sydney Institute of Marine ScienceBiology Department, San Diego State UniversityNational Center for Genome Analysis Support, Indiana UniversityBiology Department, San Diego State UniversityComputer Sciences Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityScripps Institute of Oceanography, University of California-San DiegoScripps Institute of Oceanography, University of California-San DiegoWhale Shark Mexico, ConCiencia Mexico ACBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityDepartment of Biology, University of FloridaBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityDepartment of Ecology and Evolutionary Biology, Princeton UniversityBiology Department, San Diego State UniversityBiology Department, San Diego State UniversityAbstract 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 abstracthttp://link.springer.com/article/10.1186/s40168-020-00840-xMicrobiomePhylosymbiosisMetagenomicsElasmobranch skinTeleostVertebrate fishes |