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Understanding the transition from water to land: Insights from multi-omic analyses of the perivitelline fluid of apple snail eggs.

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Title: Understanding the transition from water to land: Insights from multi-omic analyses of the perivitelline fluid of apple snail eggs.
Authors: Ip, Jack C.H.1, Mu, Huawei1, Zhang, Yanjie1, Sun, Jin1, Heras, Horacio1, Chu, Ka Hou1, Qiu, Jian-Wen1 qiujw@hkbu.edu.hk
Source: Journal of Proteomics. Mar2019, Vol. 194, p79-88. 10p.
Subjects: Gastropoda, Mollusks, Oviparity, Proteomics, Protein genetics
Abstract: Abstract Unlike most of the freshwater gastropod families, the family Ampullariidae includes members that exhibit both underwater and aerial oviposition, making it an ideal model for understanding mechanisms underlying the evolutionary transition from water to land. We applied SDS-PAGE and LC-MS/MS to analyse the proteome of the egg perivitelline fluid (PVF) of Marisa cornuarietis – an aquatic ovipositing ampullariid. Comparison with the reported PVF proteomes of two aerial ovipositing ampullariids (Pomacea canaliculata and P. maculata) showed that the three species all contain several major perivitellins that nourish the embryos. However, M. cornuarietis invests more heavily on immune-related proteins, which might be due to exposure to aquatic pathogens. Interestingly, only the PVF of out-of-water egg laying species have PV2 – a neurotoxin lethal to mice, and a calcium-binding protein which might be involved in the formation of calcareous eggshell. Integrated phylogenetic, evolutionary and gene expressional analyses detected the involvement of gene duplication, positive selection and neofunctionalisation in the formation of several major PVF proteins. Overall, our study provides multiple lines of evidence of adaptive evolution in the PVF proteins, and contributes to a better understanding of how aquatic gastropod ancestors invaded terrestrial habitats. Significance Aerial egg deposition has evolved in several groups of animals, but except for Vertebrata little is known about the mechanisms underlying this critical evolution process. We compared aquatic and aerial egg laying apple snails to understand the molecular mechanisms enabling such a transition in egg laying habitat. We found that the composition of perivitelline fluid proteomes of underwater and aerial egg depositors was remarkably different, and then gene duplication and positive selection were responsible for the formation of such novel proteins than enabled the evolutionary transition. Graphical abstract Unlabelled Image Highlights • We analyzed the perivitelline fluid proteome of a species laying eggs underwater. • We compared such proteomes of underwater and aerial egg laying species. • Underwater egg laying species invests more heavily on immune-related proteins. • Aerial egg laying species have a defence toxin and a protein for shell making. • Duplication and positive selection were involved the formation of such genes. [ABSTRACT FROM AUTHOR]
Copyright of Journal of Proteomics is the property of Elsevier B.V. and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
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  Data: Understanding the transition from water to land: Insights from multi-omic analyses of the perivitelline fluid of apple snail eggs.
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  Data: <searchLink fieldCode="AR" term="%22Ip%2C+Jack+C%2EH%2E%22">Ip, Jack C.H.</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Mu%2C+Huawei%22">Mu, Huawei</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Zhang%2C+Yanjie%22">Zhang, Yanjie</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Sun%2C+Jin%22">Sun, Jin</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Heras%2C+Horacio%22">Heras, Horacio</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Chu%2C+Ka+Hou%22">Chu, Ka Hou</searchLink><relatesTo>1</relatesTo><br /><searchLink fieldCode="AR" term="%22Qiu%2C+Jian-Wen%22">Qiu, Jian-Wen</searchLink><relatesTo>1</relatesTo><i> qiujw@hkbu.edu.hk</i>
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  Data: <searchLink fieldCode="JN" term="%22Journal+of+Proteomics%22">Journal of Proteomics</searchLink>. Mar2019, Vol. 194, p79-88. 10p.
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  Data: <searchLink fieldCode="DE" term="%22Gastropoda%22">Gastropoda</searchLink><br /><searchLink fieldCode="DE" term="%22Mollusks%22">Mollusks</searchLink><br /><searchLink fieldCode="DE" term="%22Oviparity%22">Oviparity</searchLink><br /><searchLink fieldCode="DE" term="%22Proteomics%22">Proteomics</searchLink><br /><searchLink fieldCode="DE" term="%22Protein+genetics%22">Protein genetics</searchLink>
– Name: Abstract
  Label: Abstract
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  Data: Abstract Unlike most of the freshwater gastropod families, the family Ampullariidae includes members that exhibit both underwater and aerial oviposition, making it an ideal model for understanding mechanisms underlying the evolutionary transition from water to land. We applied SDS-PAGE and LC-MS/MS to analyse the proteome of the egg perivitelline fluid (PVF) of Marisa cornuarietis – an aquatic ovipositing ampullariid. Comparison with the reported PVF proteomes of two aerial ovipositing ampullariids (Pomacea canaliculata and P. maculata) showed that the three species all contain several major perivitellins that nourish the embryos. However, M. cornuarietis invests more heavily on immune-related proteins, which might be due to exposure to aquatic pathogens. Interestingly, only the PVF of out-of-water egg laying species have PV2 – a neurotoxin lethal to mice, and a calcium-binding protein which might be involved in the formation of calcareous eggshell. Integrated phylogenetic, evolutionary and gene expressional analyses detected the involvement of gene duplication, positive selection and neofunctionalisation in the formation of several major PVF proteins. Overall, our study provides multiple lines of evidence of adaptive evolution in the PVF proteins, and contributes to a better understanding of how aquatic gastropod ancestors invaded terrestrial habitats. Significance Aerial egg deposition has evolved in several groups of animals, but except for Vertebrata little is known about the mechanisms underlying this critical evolution process. We compared aquatic and aerial egg laying apple snails to understand the molecular mechanisms enabling such a transition in egg laying habitat. We found that the composition of perivitelline fluid proteomes of underwater and aerial egg depositors was remarkably different, and then gene duplication and positive selection were responsible for the formation of such novel proteins than enabled the evolutionary transition. Graphical abstract Unlabelled Image Highlights • We analyzed the perivitelline fluid proteome of a species laying eggs underwater. • We compared such proteomes of underwater and aerial egg laying species. • Underwater egg laying species invests more heavily on immune-related proteins. • Aerial egg laying species have a defence toxin and a protein for shell making. • Duplication and positive selection were involved the formation of such genes. [ABSTRACT FROM AUTHOR]
– Name: AbstractSuppliedCopyright
  Label:
  Group: Ab
  Data: <i>Copyright of Journal of Proteomics is the property of Elsevier B.V. and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.)
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      – Type: doi
        Value: 10.1016/j.jprot.2018.12.014
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      – Code: eng
        Text: English
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        PageCount: 10
        StartPage: 79
    Subjects:
      – SubjectFull: Gastropoda
        Type: general
      – SubjectFull: Mollusks
        Type: general
      – SubjectFull: Oviparity
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      – SubjectFull: Proteomics
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      – SubjectFull: Protein genetics
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      – TitleFull: Understanding the transition from water to land: Insights from multi-omic analyses of the perivitelline fluid of apple snail eggs.
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              Text: Mar2019
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