Fish larval recruitment to reefs is a thyroid hormone-mediated metamorphosis sensitive to the pesticide chlorpyrifos

  1. Guillaume Holzer  Is a corresponding author
  2. Marc Besson  Is a corresponding author
  3. Anne Lambert
  4. Loïc François
  5. Paul Barth
  6. Benjamin Gillet
  7. Sandrine Hughes
  8. Gwenaël Piganeau
  9. Francois Leulier
  10. Laurent Viriot
  11. David Lecchini
  12. Vincent Laudet  Is a corresponding author
  1. Université de Lyon, Université Claude Bernard Lyon 1, UMR CNRS 5242, Ecole Normale Supérieure de Lyon, France
  2. PSL Research University, French Polynesia
  3. UMR CNRS 7232, Université Pierre et Marie Curie Paris, France
  4. Laboratoire d'Excellence CORAIL, French Polynesia
6 figures and 1 additional file

Figures

Figure 1 with 1 supplement
Changes in Acanthrurus triostegus during larval recruitment.

Error bars represent standard errors. *p-value<0.05; **p-value<0.01; ***p-value<0.001. (A) Schematization of the reef colonization by a larva (left) turning into a juvenile (right). The background …

https://doi.org/10.7554/eLife.27595.003
Figure 1—source data 1

Acanthurus triostegus weight at different developmental stages.

https://doi.org/10.7554/eLife.27595.005
Figure 1—source data 2

Acanthurus triostegus intestine length at different developmental stages.

https://doi.org/10.7554/eLife.27595.006
Figure 1—figure supplement 1
Changes in Acanthurus triostegus intestine and teeth during larval recruitment.

(A–O) Complete guts histology of Acanthurus triostegus after reef colonization. First column: anterior part of the intestine (first cm), middle column: medium part (variable), last column: posterior …

https://doi.org/10.7554/eLife.27595.004
Figure 2 with 3 supplements
Thyroid hormone signaling during Acanthurus triostegus metamorphosis.

Error bars represent standard errors. *p-value<0.05; **p-value<0.01; ***p-value<0.001. (A) T4 and (B) T3 dosage: Y-axis: T4 and T3 levels in pg.g−1; X-axis: sampling point. n = 3 for 5 to 10 km …

https://doi.org/10.7554/eLife.27595.007
Figure 2—source data 1

Acanthurus triostegus T4 levels in larvae and juveniles.

https://doi.org/10.7554/eLife.27595.011
Figure 2—source data 2

Acanthurus triostegus T3 levels in larvae and juveniles.

https://doi.org/10.7554/eLife.27595.012
Figure 2—source data 3

TR and Klf9 expression levels in Acanthurus triostegus at different developmental stages (qPCR).

https://doi.org/10.7554/eLife.27595.013
Figure 2—source data 4

Transactivation assay of Acanthurus triostegus TR for several thyroid hormone derivatives.

https://doi.org/10.7554/eLife.27595.014
Figure 2—source data 5

Transactivation assay of Acanthurus triostegus TR for the competition of T3 and NH3.

https://doi.org/10.7554/eLife.27595.015
Figure 2—source data 6

List of primers used in this study.

https://doi.org/10.7554/eLife.27595.016
Figure 2—source data 7

List of TR used for phylogenetic reconstruction.

https://doi.org/10.7554/eLife.27595.017
Figure 2—figure supplement 1
Characterization of Acanthurus triostegus thyroid hormone receptors.

(A) Schematic representations of TRα-A, TRα-B and TRβ from upper to lower rows respectively. The amino acid numbering of the DBD (light gray) and LBD (dark grey) appear above each TR. The nine amino …

https://doi.org/10.7554/eLife.27595.008
Figure 2—figure supplement 2
Primers used in this study.

(A) Degenerated primers used for the cloning of the A. triostegus genes in this study. (B) qPCR primers used in this study. (C) Primers used for 18S mass sequencing. The overlapping nucleotides …

https://doi.org/10.7554/eLife.27595.009
Figure 2—figure supplement 3
List of thyroid hormone receptors sequences used for the phylogeny.

Species, genes, databases and accession numbers are indicated. See Figure 2—source data 7.

https://doi.org/10.7554/eLife.27595.010
Figure 3 with 2 supplements
Impact of the environment and thyroid hormone signaling on Acanthurus triostegus metamorphic processes.

Error bars represent standard errors. *p-value<0.05; **p-value<0.01; ***p-value<0.001. (A) Upper panel: schematization of the external slope experiment with control fish, in the lagoon (grey …

https://doi.org/10.7554/eLife.27595.018
Figure 3—source data 1

T4 levels in external slope relocated Acanthus triostegus.

https://doi.org/10.7554/eLife.27595.021
Figure 3—source data 2

T3 levels in external slope relocated Acanthus triostegus.

https://doi.org/10.7554/eLife.27595.022
Figure 3—source data 3

TR and Klf9 expression levels in external slope relocated Acanthurus triostegus (qPCR).

https://doi.org/10.7554/eLife.27595.023
Figure 3—source data 4

Acanthurus triostegus intestine length under pharmacological treatments or relocation.

https://doi.org/10.7554/eLife.27595.024
Figure 3—source data 5

Acanthurus triostegus grazing activity under pharmacological treatments or relocation.

https://doi.org/10.7554/eLife.27595.025
Figure 3—figure supplement 1
Thyroid hormone signaling and environment impact on the dentition and guts histology of Acanthurus triostegus at metamorphosis.

First column: X-Ray microtomography of larva, dentition A, B or C are highlighted respectively in red, blue or green. Scale bars indicate 0.5 mm. These pictures are representative of n = 3 fish …

https://doi.org/10.7554/eLife.27595.019
Figure 3—figure supplement 2
Pigmentation patterns and thyroid hormone signaling in Acanthurus triostegus at day 2 (d2) and day (d5) during larval recruitment.

These pictures are representative of n > 10 treatment technical replicates performed on n > 100 fish (biological replicates) per treatment and per developmental stage.

https://doi.org/10.7554/eLife.27595.020
Thyroid hormone levels in distant coral reef fish at larval recruitment.

Error bars represent standard errors. *p-value<0.05; **p-value<0.01; ***p-value<0.001. TH levels of: Rhinecanthus aculeatus (upper), Chromis viridis (middle up), Chaetodon lunula (middle low) and Ost…

https://doi.org/10.7554/eLife.27595.026
Figure 4—source data 1

T4 and T3 levels of various coral reef fishes at different development stages.

https://doi.org/10.7554/eLife.27595.027
Figure 5 with 1 supplement
Influence of chlorpyrifos exposure on Acanthurus triostegus thyroid hormone signaling, intestine length, grazing activity, and algal removal efficiency.

Error bars represent standard errors. *p-value<0.05; **p-value<0.01; ***p-value<0.001. (A) T3 level in pg.g−1 of day 2 (d2) and day 5 (d5) fish exposed to different conditions: solvent control (C, …

https://doi.org/10.7554/eLife.27595.028
Figure 5—source data 1

T3 levels in Acanthurus triostegus under different chlorpyrifos exposure conditions.

https://doi.org/10.7554/eLife.27595.030
Figure 5—source data 2

Intestine length of Acanthurus triostegus under different chlorpyrifos exposure conditions.

https://doi.org/10.7554/eLife.27595.031
Figure 5—source data 3

Grazing activity of Acanthurus triostegus under different chlorpyrifos exposure conditions.

https://doi.org/10.7554/eLife.27595.032
Figure 5—source data 4

Quantity of grazed algae by Acanthurus triostegus under different chlorpyrifos exposure conditions.

https://doi.org/10.7554/eLife.27595.033
Figure 5—source data 5

T4 levels in Acanthurus triostegus under different chlorpyrifos exposure conditions.

https://doi.org/10.7554/eLife.27595.034
Figure 5—figure supplement 1
Pigmentation patterns and chlorpyrifos exposure in A. triostegus at metamorphosis.

(A) T4 level in pg.g−1 of day 2 (d2) and day 5 (d5) fish exposed to different conditions: solvent control (C, acetone, white bars), or exposed to CPF at 1 µg.l−1 (1, light yellow bars), 5 µg.l−1 (5, …

https://doi.org/10.7554/eLife.27595.029
Model of Acanthurus triostegus metamorphosis and disruption by chlorpyrifos.

(A) Schematic representation of coral reef fish larval recruitment. TH level is plotted on the Y axis and development on the X axis. The onset of metamorphosis is in the open ocean and environmental …

https://doi.org/10.7554/eLife.27595.035

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