Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia
As limits on O(2) availability during submergence impose severe constraints on aerobic respiration, the oxygen binding globin proteins of marine mammals are expected to have evolved under strong evolutionary pressures during their land-to-sea transition. Here, we address this question for the order...
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Online Access: | http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526914/ http://www.ncbi.nlm.nih.gov/pubmed/30828717 https://doi.org/10.1093/molbev/msz044 |
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ftpubmed:oai:pubmedcentral.nih.gov:6526914 2023-05-15T15:12:46+02:00 Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia Signore, Anthony V Paijmans, Johanna L A Hofreiter, Michael Fago, Angela Weber, Roy E Springer, Mark S Campbell, Kevin L 2019-06 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526914/ http://www.ncbi.nlm.nih.gov/pubmed/30828717 https://doi.org/10.1093/molbev/msz044 en eng Oxford University Press http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526914/ http://www.ncbi.nlm.nih.gov/pubmed/30828717 http://dx.doi.org/10.1093/molbev/msz044 © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com CC-BY-NC Discoveries Text 2019 ftpubmed https://doi.org/10.1093/molbev/msz044 2019-06-02T00:23:05Z As limits on O(2) availability during submergence impose severe constraints on aerobic respiration, the oxygen binding globin proteins of marine mammals are expected to have evolved under strong evolutionary pressures during their land-to-sea transition. Here, we address this question for the order Sirenia by retrieving, annotating, and performing detailed selection analyses on the globin repertoire of the extinct Steller’s sea cow (Hydrodamalis gigas), dugong (Dugong dugon), and Florida manatee (Trichechus manatus latirostris) in relation to their closest living terrestrial relatives (elephants and hyraxes). These analyses indicate most loci experienced elevated nucleotide substitution rates during their transition to a fully aquatic lifestyle. While most of these genes evolved under neutrality or strong purifying selection, the rate of nonsynonymous/synonymous replacements increased in two genes (Hbz-T1 and Hba-T1) that encode the α-type chains of hemoglobin (Hb) during each stage of life. Notably, the relaxed evolution of Hba-T1 is temporally coupled with the emergence of a chimeric pseudogene (Hba-T2/Hbq-ps) that contributed to the tandemly linked Hba-T1 of stem sirenians via interparalog gene conversion. Functional tests on recombinant Hb proteins from extant and ancestral sirenians further revealed that the molecular remodeling of Hba-T1 coincided with increased Hb–O(2) affinity in early sirenians. Available evidence suggests that this trait evolved to maximize O(2) extraction from finite lung stores and suppress tissue O(2) offloading, thereby facilitating the low metabolic intensities of extant sirenians. In contrast, the derived reduction in Hb–O(2) affinity in (sub)Arctic Steller’s sea cows is consistent with fueling increased thermogenesis by these once colossal marine herbivores. Text Arctic Hydrodamalis gigas PubMed Central (PMC) Arctic Molecular Biology and Evolution 36 6 1134 1147 |
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Discoveries Signore, Anthony V Paijmans, Johanna L A Hofreiter, Michael Fago, Angela Weber, Roy E Springer, Mark S Campbell, Kevin L Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia |
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Discoveries |
description |
As limits on O(2) availability during submergence impose severe constraints on aerobic respiration, the oxygen binding globin proteins of marine mammals are expected to have evolved under strong evolutionary pressures during their land-to-sea transition. Here, we address this question for the order Sirenia by retrieving, annotating, and performing detailed selection analyses on the globin repertoire of the extinct Steller’s sea cow (Hydrodamalis gigas), dugong (Dugong dugon), and Florida manatee (Trichechus manatus latirostris) in relation to their closest living terrestrial relatives (elephants and hyraxes). These analyses indicate most loci experienced elevated nucleotide substitution rates during their transition to a fully aquatic lifestyle. While most of these genes evolved under neutrality or strong purifying selection, the rate of nonsynonymous/synonymous replacements increased in two genes (Hbz-T1 and Hba-T1) that encode the α-type chains of hemoglobin (Hb) during each stage of life. Notably, the relaxed evolution of Hba-T1 is temporally coupled with the emergence of a chimeric pseudogene (Hba-T2/Hbq-ps) that contributed to the tandemly linked Hba-T1 of stem sirenians via interparalog gene conversion. Functional tests on recombinant Hb proteins from extant and ancestral sirenians further revealed that the molecular remodeling of Hba-T1 coincided with increased Hb–O(2) affinity in early sirenians. Available evidence suggests that this trait evolved to maximize O(2) extraction from finite lung stores and suppress tissue O(2) offloading, thereby facilitating the low metabolic intensities of extant sirenians. In contrast, the derived reduction in Hb–O(2) affinity in (sub)Arctic Steller’s sea cows is consistent with fueling increased thermogenesis by these once colossal marine herbivores. |
format |
Text |
author |
Signore, Anthony V Paijmans, Johanna L A Hofreiter, Michael Fago, Angela Weber, Roy E Springer, Mark S Campbell, Kevin L |
author_facet |
Signore, Anthony V Paijmans, Johanna L A Hofreiter, Michael Fago, Angela Weber, Roy E Springer, Mark S Campbell, Kevin L |
author_sort |
Signore, Anthony V |
title |
Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia |
title_short |
Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia |
title_full |
Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia |
title_fullStr |
Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia |
title_full_unstemmed |
Emergence of a Chimeric Globin Pseudogene and Increased Hemoglobin Oxygen Affinity Underlie the Evolution of Aquatic Specializations in Sirenia |
title_sort |
emergence of a chimeric globin pseudogene and increased hemoglobin oxygen affinity underlie the evolution of aquatic specializations in sirenia |
publisher |
Oxford University Press |
publishDate |
2019 |
url |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526914/ http://www.ncbi.nlm.nih.gov/pubmed/30828717 https://doi.org/10.1093/molbev/msz044 |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic Hydrodamalis gigas |
genre_facet |
Arctic Hydrodamalis gigas |
op_relation |
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526914/ http://www.ncbi.nlm.nih.gov/pubmed/30828717 http://dx.doi.org/10.1093/molbev/msz044 |
op_rights |
© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com |
op_rightsnorm |
CC-BY-NC |
op_doi |
https://doi.org/10.1093/molbev/msz044 |
container_title |
Molecular Biology and Evolution |
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36 |
container_issue |
6 |
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1134 |
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1147 |
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1766343414748545024 |