The University of Southampton
University of Southampton Institutional Repository

Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics

Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics
Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics

Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO3 crystals form complex biocomposites with proteins, which although typically less than 5% of total shell mass, play significant roles in determining shell microstructure. Despite much research effort, large knowledge gaps remain in how molluscs construct and maintain their shells, and how they produce such a great diversity of forms. Here we synthesize results on how shell shape, microstructure, composition and organic content vary among, and within, species in response to numerous biotic and abiotic factors. At the local level, temperature, food supply and predation cues significantly affect shell morphology, whilst salinity has a much stronger influence across latitudes. Moreover, we emphasize how advances in genomic technologies [e.g. restriction site-associated DNA sequencing (RAD-Seq) and epigenetics] allow detailed examinations of whether morphological changes result from phenotypic plasticity or genetic adaptation, or a combination of these. RAD-Seq has already identified single nucleotide polymorphisms associated with temperature and aquaculture practices, whilst epigenetic processes have been shown significantly to modify shell construction to local conditions in, for example, Antarctica and New Zealand. We also synthesize results on the costs of shell construction and explore how these affect energetic trade-offs in animal metabolism. The cellular costs are still debated, with CaCO3 precipitation estimates ranging from 1-2 J/mg to 17-55 J/mg depending on experimental and environmental conditions. However, organic components are more expensive (~29 J/mg) and recent data indicate transmembrane calcium ion transporters can involve considerable costs. This review emphasizes the role that molecular analyses have played in demonstrating multiple evolutionary origins of biomineralization genes. Although these are characterized by lineage-specific proteins and unique combinations of co-opted genes, a small set of protein domains have been identified as a conserved biomineralization tool box. We further highlight the use of sequence data sets in providing candidate genes for in situ localization and protein function studies. The former has elucidated gene expression modularity in mantle tissue, improving understanding of the diversity of shell morphology synthesis. RNA interference (RNAi) and clustered regularly interspersed short palindromic repeats - CRISPR-associated protein 9 (CRISPR-Cas9) experiments have provided proof of concept for use in the functional investigation of mollusc gene sequences, showing for example that Pif (aragonite-binding) protein plays a significant role in structured nacre crystal growth and that the Lsdia1 gene sets shell chirality in Lymnaea stagnalis. Much research has focused on the impacts of ocean acidification on molluscs. Initial studies were predominantly pessimistic for future molluscan biodiversity. However, more sophisticated experiments incorporating selective breeding and multiple generations are identifying subtle effects and that variability within mollusc genomes has potential for adaption to future conditions. Furthermore, we highlight recent historical studies based on museum collections that demonstrate a greater resilience of molluscs to climate change compared with experimental data. The future of mollusc research lies not solely with ecological investigations into biodiversity, and this review synthesizes knowledge across disciplines to understand biomineralization. It spans research ranging from evolution and development, through predictions of biodiversity prospects and future-proofing of aquaculture to identifying new biomimetic opportunities and societal benefits from recycling shell products.

1464-7931
1812-1837
Clark, Melody S
ddff611b-5d72-4144-b399-6d7c5ccb732b
Peck, Lloyd S
097d27ed-4644-4bc1-a855-045029ace2df
Arivalagan, Jaison
320a6e81-f0be-4a9a-ad04-56521a3a49e7
Backeljau, Thierry
a6e53e80-77b5-4083-aebf-cd441acf8eab
Berland, Sophie
0385d953-667a-4440-95f4-100bfd069ddc
Cardoso, Joao C R
eef12169-d408-4fa6-846c-f978d1a6cd93
Caurcel, Carlos
e80799d0-7e23-4dfa-ab29-74af3fe72512
Chapelle, Gauthier
baab0228-d38d-438d-b3d8-eab180d18a3f
De Noia, Michele
0b4a1074-83e3-45fa-8cf8-f7ae76a83a5b
Dupont, Sam
9c78aeab-1e9e-459a-a0aa-698bf8234c87
Gharbi, Karim
9715391a-8b72-4075-9ca3-3176f5c66b09
Hoffman, Joseph I
96ca2704-4ff3-4ef8-9159-253418ef60de
Last, Kim S
5132c1c6-c15d-46e9-9fe0-ab0dd8fdb98b
Marie, Arul
b962efc6-f4d6-499e-96d8-84de4cf57d35
Melzner, Frank
c95fbb6b-6721-4f38-a22e-2408e9400868
Michalek, Kati
471d381b-c1c7-4122-b563-72afa6e97454
Morris, James
7060ae12-d0fd-41a5-89df-83870b59be31
Power, Deborah M
96dc370f-0efb-42ab-bb89-55767f2bf1ea
Ramesh, Kirti
c67662b4-1444-41a6-a53f-c3986e6d07b1
Sanders, Trystan
4f3b5742-82bb-48d6-bcaa-0489c0880628
Sillanpää, Kirsikka
8654f651-48d4-4b5c-a70b-613525473e46
Sleight, Victoria A
163d5cc9-cb6f-4fb3-aa8b-fcea1b1a9916
Stewart-Sinclair, Phoebe J
9925c811-c0d5-4953-9b5f-417eff2f572b
Sundell, Kristina
bf8c0bfc-0a73-462a-9699-84220168bb8f
Telesca, Luca
ece9af91-8459-4151-b9f8-fdff453142ce
Vendrami, David L J
36465175-eda3-4b4f-8b82-e72d9c7d9341
Ventura, Alexander
50496a9d-6abb-4388-8877-804bdf7b14d3
Wilding, Thomas A
0449b8ef-e80b-4359-ac82-3dab9cee2616
Yarra, Tejaswi
98d8b637-b4ca-4dd1-9a05-354700690cdc
Harper, Elizabeth M
a365be7f-8523-43e2-a102-720eaed6c856
Clark, Melody S
ddff611b-5d72-4144-b399-6d7c5ccb732b
Peck, Lloyd S
097d27ed-4644-4bc1-a855-045029ace2df
Arivalagan, Jaison
320a6e81-f0be-4a9a-ad04-56521a3a49e7
Backeljau, Thierry
a6e53e80-77b5-4083-aebf-cd441acf8eab
Berland, Sophie
0385d953-667a-4440-95f4-100bfd069ddc
Cardoso, Joao C R
eef12169-d408-4fa6-846c-f978d1a6cd93
Caurcel, Carlos
e80799d0-7e23-4dfa-ab29-74af3fe72512
Chapelle, Gauthier
baab0228-d38d-438d-b3d8-eab180d18a3f
De Noia, Michele
0b4a1074-83e3-45fa-8cf8-f7ae76a83a5b
Dupont, Sam
9c78aeab-1e9e-459a-a0aa-698bf8234c87
Gharbi, Karim
9715391a-8b72-4075-9ca3-3176f5c66b09
Hoffman, Joseph I
96ca2704-4ff3-4ef8-9159-253418ef60de
Last, Kim S
5132c1c6-c15d-46e9-9fe0-ab0dd8fdb98b
Marie, Arul
b962efc6-f4d6-499e-96d8-84de4cf57d35
Melzner, Frank
c95fbb6b-6721-4f38-a22e-2408e9400868
Michalek, Kati
471d381b-c1c7-4122-b563-72afa6e97454
Morris, James
7060ae12-d0fd-41a5-89df-83870b59be31
Power, Deborah M
96dc370f-0efb-42ab-bb89-55767f2bf1ea
Ramesh, Kirti
c67662b4-1444-41a6-a53f-c3986e6d07b1
Sanders, Trystan
4f3b5742-82bb-48d6-bcaa-0489c0880628
Sillanpää, Kirsikka
8654f651-48d4-4b5c-a70b-613525473e46
Sleight, Victoria A
163d5cc9-cb6f-4fb3-aa8b-fcea1b1a9916
Stewart-Sinclair, Phoebe J
9925c811-c0d5-4953-9b5f-417eff2f572b
Sundell, Kristina
bf8c0bfc-0a73-462a-9699-84220168bb8f
Telesca, Luca
ece9af91-8459-4151-b9f8-fdff453142ce
Vendrami, David L J
36465175-eda3-4b4f-8b82-e72d9c7d9341
Ventura, Alexander
50496a9d-6abb-4388-8877-804bdf7b14d3
Wilding, Thomas A
0449b8ef-e80b-4359-ac82-3dab9cee2616
Yarra, Tejaswi
98d8b637-b4ca-4dd1-9a05-354700690cdc
Harper, Elizabeth M
a365be7f-8523-43e2-a102-720eaed6c856

Clark, Melody S, Peck, Lloyd S, Arivalagan, Jaison, Backeljau, Thierry, Berland, Sophie, Cardoso, Joao C R, Caurcel, Carlos, Chapelle, Gauthier, De Noia, Michele, Dupont, Sam, Gharbi, Karim, Hoffman, Joseph I, Last, Kim S, Marie, Arul, Melzner, Frank, Michalek, Kati, Morris, James, Power, Deborah M, Ramesh, Kirti, Sanders, Trystan, Sillanpää, Kirsikka, Sleight, Victoria A, Stewart-Sinclair, Phoebe J, Sundell, Kristina, Telesca, Luca, Vendrami, David L J, Ventura, Alexander, Wilding, Thomas A, Yarra, Tejaswi and Harper, Elizabeth M (2020) Deciphering mollusc shell production: the roles of genetic mechanisms through to ecology, aquaculture and biomimetics. Biological Reviews, 95 (6), 1812-1837. (doi:10.1111/brv.12640).

Record type: Article

Abstract

Most molluscs possess shells, constructed from a vast array of microstructures and architectures. The fully formed shell is composed of calcite or aragonite. These CaCO3 crystals form complex biocomposites with proteins, which although typically less than 5% of total shell mass, play significant roles in determining shell microstructure. Despite much research effort, large knowledge gaps remain in how molluscs construct and maintain their shells, and how they produce such a great diversity of forms. Here we synthesize results on how shell shape, microstructure, composition and organic content vary among, and within, species in response to numerous biotic and abiotic factors. At the local level, temperature, food supply and predation cues significantly affect shell morphology, whilst salinity has a much stronger influence across latitudes. Moreover, we emphasize how advances in genomic technologies [e.g. restriction site-associated DNA sequencing (RAD-Seq) and epigenetics] allow detailed examinations of whether morphological changes result from phenotypic plasticity or genetic adaptation, or a combination of these. RAD-Seq has already identified single nucleotide polymorphisms associated with temperature and aquaculture practices, whilst epigenetic processes have been shown significantly to modify shell construction to local conditions in, for example, Antarctica and New Zealand. We also synthesize results on the costs of shell construction and explore how these affect energetic trade-offs in animal metabolism. The cellular costs are still debated, with CaCO3 precipitation estimates ranging from 1-2 J/mg to 17-55 J/mg depending on experimental and environmental conditions. However, organic components are more expensive (~29 J/mg) and recent data indicate transmembrane calcium ion transporters can involve considerable costs. This review emphasizes the role that molecular analyses have played in demonstrating multiple evolutionary origins of biomineralization genes. Although these are characterized by lineage-specific proteins and unique combinations of co-opted genes, a small set of protein domains have been identified as a conserved biomineralization tool box. We further highlight the use of sequence data sets in providing candidate genes for in situ localization and protein function studies. The former has elucidated gene expression modularity in mantle tissue, improving understanding of the diversity of shell morphology synthesis. RNA interference (RNAi) and clustered regularly interspersed short palindromic repeats - CRISPR-associated protein 9 (CRISPR-Cas9) experiments have provided proof of concept for use in the functional investigation of mollusc gene sequences, showing for example that Pif (aragonite-binding) protein plays a significant role in structured nacre crystal growth and that the Lsdia1 gene sets shell chirality in Lymnaea stagnalis. Much research has focused on the impacts of ocean acidification on molluscs. Initial studies were predominantly pessimistic for future molluscan biodiversity. However, more sophisticated experiments incorporating selective breeding and multiple generations are identifying subtle effects and that variability within mollusc genomes has potential for adaption to future conditions. Furthermore, we highlight recent historical studies based on museum collections that demonstrate a greater resilience of molluscs to climate change compared with experimental data. The future of mollusc research lies not solely with ecological investigations into biodiversity, and this review synthesizes knowledge across disciplines to understand biomineralization. It spans research ranging from evolution and development, through predictions of biodiversity prospects and future-proofing of aquaculture to identifying new biomimetic opportunities and societal benefits from recycling shell products.

Text
brv.12640 - Version of Record
Available under License Creative Commons Attribution.
Download (4MB)

More information

e-pub ahead of print date: 31 July 2020
Published date: December 2020

Identifiers

Local EPrints ID: 448577
URI: http://eprints.soton.ac.uk/id/eprint/448577
ISSN: 1464-7931
PURE UUID: 948784aa-f2e7-4a12-85b9-74be313b14ba
ORCID for Trystan Sanders: ORCID iD orcid.org/0000-0002-7605-0747

Catalogue record

Date deposited: 27 Apr 2021 16:43
Last modified: 24 Nov 2022 03:02

Export record

Altmetrics

Contributors

Author: Melody S Clark
Author: Lloyd S Peck
Author: Jaison Arivalagan
Author: Thierry Backeljau
Author: Sophie Berland
Author: Joao C R Cardoso
Author: Carlos Caurcel
Author: Gauthier Chapelle
Author: Michele De Noia
Author: Sam Dupont
Author: Karim Gharbi
Author: Joseph I Hoffman
Author: Kim S Last
Author: Arul Marie
Author: Frank Melzner
Author: Kati Michalek
Author: James Morris
Author: Deborah M Power
Author: Kirti Ramesh
Author: Trystan Sanders ORCID iD
Author: Kirsikka Sillanpää
Author: Victoria A Sleight
Author: Phoebe J Stewart-Sinclair
Author: Kristina Sundell
Author: Luca Telesca
Author: David L J Vendrami
Author: Alexander Ventura
Author: Thomas A Wilding
Author: Tejaswi Yarra
Author: Elizabeth M Harper

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×