Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement

Abstract Introduction Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with...

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Main Authors: Paula Suarez-Bregua, Sofia Rosendo, Pilar Comesaña, Lucia Sánchez-Ruiloba, Paloma Morán, Miquel Planas, Josep Rotllant
Format: Article
Language:English
Published: BMC 2021-10-01
Series:Frontiers in Zoology
Subjects:
Online Access:https://doi.org/10.1186/s12983-021-00436-7
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spelling doaj-8c983d94287b4a7aa8ddaa9f30bfb5a72021-10-10T11:37:13ZengBMCFrontiers in Zoology1742-99942021-10-0118111010.1186/s12983-021-00436-7Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlementPaula Suarez-Bregua0Sofia Rosendo1Pilar Comesaña2Lucia Sánchez-Ruiloba3Paloma Morán4Miquel Planas5Josep Rotllant6Acuatic Biotechnology-ACUABIOTEC Lab, Department of Biotechnology and Aquaculture, Marine Research Institute IIM-CSICAcuatic Biotechnology-ACUABIOTEC Lab, Department of Biotechnology and Aquaculture, Marine Research Institute IIM-CSICAcuatic Biotechnology-ACUABIOTEC Lab, Department of Biotechnology and Aquaculture, Marine Research Institute IIM-CSICAcuatic Biotechnology-ACUABIOTEC Lab, Department of Biotechnology and Aquaculture, Marine Research Institute IIM-CSICDepartment of Biochemistry, Genetics and Immunology, University of VigoDepartment of Ecology and Marine Resources, Marine Research Institute IIM-CSICAcuatic Biotechnology-ACUABIOTEC Lab, Department of Biotechnology and Aquaculture, Marine Research Institute IIM-CSICAbstract Introduction Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with the ecological transition from a pelagic to a benthonic lifestyle. Therefore, transition from a pelagic to a benthonic habitat requires multiple adaptations, however, the underlying mechanisms regulating this process still remains unclear. Epigenetic regulation and specifically DNA methylation, has been suggested to be particularly important for organisms to adapt to new environments. Seahorses (Family Syngnathidae, Genus Hippocampus) are a fascinating group of fish, distinguished by their unique anatomical features, reproductive strategy and behavior. They are unique among vertebrate species due to their “male pregnancy”, where males nourish developing embryos and larvae in a brood pouch until hatching and parturition occurs. After birth, free-swimming offspring are pelagic and subsequently they change into a demersal lifestyle. Therefore, to begin to address the question whether epigenetic processes could be involved in the transition from a planktonic to a benthonic lifestyle observed in seahorses, we studied global DNA methylation profiles in a tropical seahorse species (Hippocampus reidi) during postnatal development and settlement. Results We performed methylation-sensitive amplified polymorphism (MSAP) along with quantitative expression analysis for genes suggested to be involved in the methylation machinery at six age groups: 1, 5, 10, 20, 30 and 40 days after male’s pouch release (DAR). Results revealed that the H. reidi genome has a significantly different DNA methylation profile during postnatal development and settlement on demersal habitats. Moreover, gene expression analysis showed up- and down-regulation of specific DNA methyltransferases (DNMTs) encoding genes. Conclusion Our data show that the differences in the DNA methylation patterns seen among developmental stages and during the transition from a pelagic to a benthonic lifestyle suggest a potential for epigenetic regulation of gene expression (through DNA methylation) in this species. Therefore, epigenetic mechanisms could be necessary for seahorse settlement. Nevertheless, if these epigenetic mechanisms come from internal or if they are initiated via external environmental cues should be further investigated.https://doi.org/10.1186/s12983-021-00436-7SeahorseHippocampusDNA methylationSettlementMSAP analysis
collection DOAJ
language English
format Article
sources DOAJ
author Paula Suarez-Bregua
Sofia Rosendo
Pilar Comesaña
Lucia Sánchez-Ruiloba
Paloma Morán
Miquel Planas
Josep Rotllant
spellingShingle Paula Suarez-Bregua
Sofia Rosendo
Pilar Comesaña
Lucia Sánchez-Ruiloba
Paloma Morán
Miquel Planas
Josep Rotllant
Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
Frontiers in Zoology
Seahorse
Hippocampus
DNA methylation
Settlement
MSAP analysis
author_facet Paula Suarez-Bregua
Sofia Rosendo
Pilar Comesaña
Lucia Sánchez-Ruiloba
Paloma Morán
Miquel Planas
Josep Rotllant
author_sort Paula Suarez-Bregua
title Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_short Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_full Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_fullStr Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_full_unstemmed Dynamic changes in DNA methylation during seahorse (Hippocampus reidi) postnatal development and settlement
title_sort dynamic changes in dna methylation during seahorse (hippocampus reidi) postnatal development and settlement
publisher BMC
series Frontiers in Zoology
issn 1742-9994
publishDate 2021-10-01
description Abstract Introduction Most living marine organisms have a biphasic life cycle dependent on metamorphosis and settlement. These critical life-history events mean that a developmentally competent larva undergoes a range of coordinated morphological and physiological changes that are in synchrony with the ecological transition from a pelagic to a benthonic lifestyle. Therefore, transition from a pelagic to a benthonic habitat requires multiple adaptations, however, the underlying mechanisms regulating this process still remains unclear. Epigenetic regulation and specifically DNA methylation, has been suggested to be particularly important for organisms to adapt to new environments. Seahorses (Family Syngnathidae, Genus Hippocampus) are a fascinating group of fish, distinguished by their unique anatomical features, reproductive strategy and behavior. They are unique among vertebrate species due to their “male pregnancy”, where males nourish developing embryos and larvae in a brood pouch until hatching and parturition occurs. After birth, free-swimming offspring are pelagic and subsequently they change into a demersal lifestyle. Therefore, to begin to address the question whether epigenetic processes could be involved in the transition from a planktonic to a benthonic lifestyle observed in seahorses, we studied global DNA methylation profiles in a tropical seahorse species (Hippocampus reidi) during postnatal development and settlement. Results We performed methylation-sensitive amplified polymorphism (MSAP) along with quantitative expression analysis for genes suggested to be involved in the methylation machinery at six age groups: 1, 5, 10, 20, 30 and 40 days after male’s pouch release (DAR). Results revealed that the H. reidi genome has a significantly different DNA methylation profile during postnatal development and settlement on demersal habitats. Moreover, gene expression analysis showed up- and down-regulation of specific DNA methyltransferases (DNMTs) encoding genes. Conclusion Our data show that the differences in the DNA methylation patterns seen among developmental stages and during the transition from a pelagic to a benthonic lifestyle suggest a potential for epigenetic regulation of gene expression (through DNA methylation) in this species. Therefore, epigenetic mechanisms could be necessary for seahorse settlement. Nevertheless, if these epigenetic mechanisms come from internal or if they are initiated via external environmental cues should be further investigated.
topic Seahorse
Hippocampus
DNA methylation
Settlement
MSAP analysis
url https://doi.org/10.1186/s12983-021-00436-7
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