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Molecular and biochemical basis for the loss of bioluminescence in the inoflagellate Noctiluca scintillans along the west coast of the U.S.A.

Molecular and biochemical basis for the loss of bioluminescence in the inoflagellate Noctiluca scintillans along the west coast of the U.S.A.
Molecular and biochemical basis for the loss of bioluminescence in the inoflagellate Noctiluca scintillans along the west coast of the U.S.A.
The globally distributed heterotrophic dinoflagellate Noctiluca scintillans (Macartney) Kofoid & Swezy is well known for its dense blooms and prominent displays of bioluminescence. Intriguingly, along the west coast of the U.S.A., its blooms are not bioluminescent. We investigated the basis for this regional loss of bioluminescence using molecular, cellular, and biochemical analyses of isolates from different geographic regions. Several prominent differences were identified in the nonbioluminescent strains: (1) the fused luciferase and luciferin binding protein gene (lcf/lbp) was present but its transcripts were undetectable; (2) lcf/lbp contained multiple potentially deleterious mutations; (3) the substrate luciferin was absent, based on the lack of luciferin blue autofluorescence and the absence of luciferin‐derived metabolites; (4) although the cells possessed scintillons, the organelles that contain the luminescent chemistry, electron microscopy revealed additional scintillon‐like organelles with an atypical internal structure; and (5) cells isolated from the California coast were 43% smaller than bioluminescent cells from the Gulf of Mexico. Phylogenetic analyses based on large subunit rDNA did not show divergence of the nonbioluminescent population in relation to bioluminescent N. scintillans from the Pacific Ocean and Arabian Sea. This study demonstrates that gene silencing and the lack of the luciferin substrate have resulted in the loss of an important dinoflagellate functional trait over large spatial scales in the ocean. As the bioluminescence system of dinoflagellates is well characterized, nonbioluminescent N. scintillans provide an ideal model to explore the evolutionary and ecological mechanisms that lead to intraspecific functional divergence in natural dinoflagellate populations.
0024-3590
1-16
Valiadi, Martha
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Rond, Tristan
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Amorim, Ana
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Gittins, John R.
c4d269cc-aae0-4182-bc81-78dc724f7d95
Gubili, Chrysoula
2e1c2861-97f0-4fff-9f38-f76985defd49
Moore, Bradley S.
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Iglesias‐rodriguez, Maria Debora
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Latz, Michael I.
3df40be8-2e91-4f38-aba0-2c20a0a9d8e6
Valiadi, Martha
e245e9c5-3e97-4896-b910-c4178c5fb3c9
Rond, Tristan
b6c44698-2274-4257-9570-af448106ea9c
Amorim, Ana
c04f0ebc-3c84-4614-be7d-0aa2580f1ebb
Gittins, John R.
c4d269cc-aae0-4182-bc81-78dc724f7d95
Gubili, Chrysoula
2e1c2861-97f0-4fff-9f38-f76985defd49
Moore, Bradley S.
43a4be00-16a1-4f98-8325-ff87fa8bd83f
Iglesias‐rodriguez, Maria Debora
8255cec6-8848-472d-97b4-1e86ab59b251
Latz, Michael I.
3df40be8-2e91-4f38-aba0-2c20a0a9d8e6

Valiadi, Martha, Rond, Tristan, Amorim, Ana, Gittins, John R., Gubili, Chrysoula, Moore, Bradley S., Iglesias‐rodriguez, Maria Debora and Latz, Michael I. (2019) Molecular and biochemical basis for the loss of bioluminescence in the inoflagellate Noctiluca scintillans along the west coast of the U.S.A. Limnology and Oceanography, 1-16. (doi:10.1002/lno.11309).

Record type: Article

Abstract

The globally distributed heterotrophic dinoflagellate Noctiluca scintillans (Macartney) Kofoid & Swezy is well known for its dense blooms and prominent displays of bioluminescence. Intriguingly, along the west coast of the U.S.A., its blooms are not bioluminescent. We investigated the basis for this regional loss of bioluminescence using molecular, cellular, and biochemical analyses of isolates from different geographic regions. Several prominent differences were identified in the nonbioluminescent strains: (1) the fused luciferase and luciferin binding protein gene (lcf/lbp) was present but its transcripts were undetectable; (2) lcf/lbp contained multiple potentially deleterious mutations; (3) the substrate luciferin was absent, based on the lack of luciferin blue autofluorescence and the absence of luciferin‐derived metabolites; (4) although the cells possessed scintillons, the organelles that contain the luminescent chemistry, electron microscopy revealed additional scintillon‐like organelles with an atypical internal structure; and (5) cells isolated from the California coast were 43% smaller than bioluminescent cells from the Gulf of Mexico. Phylogenetic analyses based on large subunit rDNA did not show divergence of the nonbioluminescent population in relation to bioluminescent N. scintillans from the Pacific Ocean and Arabian Sea. This study demonstrates that gene silencing and the lack of the luciferin substrate have resulted in the loss of an important dinoflagellate functional trait over large spatial scales in the ocean. As the bioluminescence system of dinoflagellates is well characterized, nonbioluminescent N. scintillans provide an ideal model to explore the evolutionary and ecological mechanisms that lead to intraspecific functional divergence in natural dinoflagellate populations.

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Valiadi LO submission proof 10 Jun 2019 - Accepted Manuscript
Restricted to Repository staff only until 19 October 2020.
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Accepted/In Press date: 16 July 2019
e-pub ahead of print date: 19 August 2019

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Local EPrints ID: 434935
URI: https://eprints.soton.ac.uk/id/eprint/434935
ISSN: 0024-3590
PURE UUID: c0ab565d-45be-44c8-a770-0543d44279e1

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Date deposited: 16 Oct 2019 16:30
Last modified: 16 Oct 2019 16:30

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Contributors

Author: Martha Valiadi
Author: Tristan Rond
Author: Ana Amorim
Author: John R. Gittins
Author: Chrysoula Gubili
Author: Bradley S. Moore
Author: Maria Debora Iglesias‐rodriguez
Author: Michael I. Latz

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