Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans

Abstract Cetaceans are a unique group of marine mammals that have evolved from terrestrial to fully aquatic life. During diving, they experience extreme physiological challenges, including lung collapse, limited gas exchange, and the risk of decompression-related injuries. The matrix metalloproteina...

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Main Authors: Ya Zhang, Wenjun Lv, Wen Yan, Boxiong Guo, Guang Yang, Wenhua Ren
Format: Article
Language:English
Published: BMC 2025-06-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11751-2
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author Ya Zhang
Wenjun Lv
Wen Yan
Boxiong Guo
Guang Yang
Wenhua Ren
author_facet Ya Zhang
Wenjun Lv
Wen Yan
Boxiong Guo
Guang Yang
Wenhua Ren
author_sort Ya Zhang
collection DOAJ
description Abstract Cetaceans are a unique group of marine mammals that have evolved from terrestrial to fully aquatic life. During diving, they experience extreme physiological challenges, including lung collapse, limited gas exchange, and the risk of decompression-related injuries. The matrix metalloproteinase (MMP) gene family plays a central role in extracellular matrix (ECM) remodeling, vascular repair, and inflammatory responses, and is also involved in the formation and maintenance of elastic fibers—key components that contribute to lung elasticity. Enhanced lung elasticity is thought to facilitate reversible lung collapse and efficient blood shift during dives, ultimately reducing nitrogen uptake and the potential risk of decompression sickness (DCS). In this study, we analyzed 1,058 genes from 46 species, focusing on cetaceans and other diving marine mammals, with terrestrial mammals as a reference group. Our results reveal that the MMP gene family has undergone positive selection in cetaceans, with nine genes exhibiting accelerated evolution. Notably, we identified a cetacean-specific N319S mutation in the Fibronectin type-II domain of MMP9, which impairs collagen-binding and degradation, as confirmed by Western blot analysis. Mass spectrometry further revealed an increased number of post-translational modifications in cetacean MMP9 compared to terrestrial mammals, with several modifications overlapping the mutation sites. These findings suggest that adaptive changes in MMPs may enhance elastic fiber dynamics and vascular remodeling in cetaceans, contributing to physiological adaptations such as improved lung compliance and resilience to diving-related stress, including reduced susceptibility to DCS.
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spelling doaj-art-7bc22f1444bb46d1ab90d056fb96e1752025-08-20T03:31:42ZengBMCBMC Genomics1471-21642025-06-0126111510.1186/s12864-025-11751-2Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceansYa Zhang0Wenjun Lv1Wen Yan2Boxiong Guo3Guang Yang4Wenhua Ren5Jiangsu Key Laboratory for the Biodiversity Conservation and Sustainable Utilization in the Middle and Lower Reaches of the Yangtze River Basin, College of Life Sciences, Nanjing Normal UniversityJiangsu Key Laboratory for the Biodiversity Conservation and Sustainable Utilization in the Middle and Lower Reaches of the Yangtze River Basin, College of Life Sciences, Nanjing Normal UniversityJiangsu Key Laboratory for the Biodiversity Conservation and Sustainable Utilization in the Middle and Lower Reaches of the Yangtze River Basin, College of Life Sciences, Nanjing Normal UniversityInstitute of Entomology, College of Life Sciences, Nankai UniversityJiangsu Key Laboratory for the Biodiversity Conservation and Sustainable Utilization in the Middle and Lower Reaches of the Yangtze River Basin, College of Life Sciences, Nanjing Normal UniversityJiangsu Key Laboratory for the Biodiversity Conservation and Sustainable Utilization in the Middle and Lower Reaches of the Yangtze River Basin, College of Life Sciences, Nanjing Normal UniversityAbstract Cetaceans are a unique group of marine mammals that have evolved from terrestrial to fully aquatic life. During diving, they experience extreme physiological challenges, including lung collapse, limited gas exchange, and the risk of decompression-related injuries. The matrix metalloproteinase (MMP) gene family plays a central role in extracellular matrix (ECM) remodeling, vascular repair, and inflammatory responses, and is also involved in the formation and maintenance of elastic fibers—key components that contribute to lung elasticity. Enhanced lung elasticity is thought to facilitate reversible lung collapse and efficient blood shift during dives, ultimately reducing nitrogen uptake and the potential risk of decompression sickness (DCS). In this study, we analyzed 1,058 genes from 46 species, focusing on cetaceans and other diving marine mammals, with terrestrial mammals as a reference group. Our results reveal that the MMP gene family has undergone positive selection in cetaceans, with nine genes exhibiting accelerated evolution. Notably, we identified a cetacean-specific N319S mutation in the Fibronectin type-II domain of MMP9, which impairs collagen-binding and degradation, as confirmed by Western blot analysis. Mass spectrometry further revealed an increased number of post-translational modifications in cetacean MMP9 compared to terrestrial mammals, with several modifications overlapping the mutation sites. These findings suggest that adaptive changes in MMPs may enhance elastic fiber dynamics and vascular remodeling in cetaceans, contributing to physiological adaptations such as improved lung compliance and resilience to diving-related stress, including reduced susceptibility to DCS.https://doi.org/10.1186/s12864-025-11751-2Convergent evolutionPulmonary fibrosisDiving adaptationsMarine mammals
spellingShingle Ya Zhang
Wenjun Lv
Wen Yan
Boxiong Guo
Guang Yang
Wenhua Ren
Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans
BMC Genomics
Convergent evolution
Pulmonary fibrosis
Diving adaptations
Marine mammals
title Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans
title_full Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans
title_fullStr Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans
title_full_unstemmed Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans
title_short Molecular adaptations in MMP genes support lung elasticity and diving adaptations in cetaceans
title_sort molecular adaptations in mmp genes support lung elasticity and diving adaptations in cetaceans
topic Convergent evolution
Pulmonary fibrosis
Diving adaptations
Marine mammals
url https://doi.org/10.1186/s12864-025-11751-2
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