Research ArticleORGANISMAL BIOLOGY

A new case of kleptoplasty in animals: Marine flatworms steal functional plastids from diatoms

See allHide authors and affiliations

Science Advances  17 Jul 2019:
Vol. 5, no. 7, eaaw4337
DOI: 10.1126/sciadv.aaw4337
  • Fig. 1 Light, fluorescence, and transmission electron micrographs of B. solaris and its kleptoplasts.

    (A) Live specimen with eyes (arrow), pharynx, and golden-brown kleptoplasts; darker plastids are being degraded. (B) Kleptoplasts and empty frustules of pennate diatoms (large black arrowheads). (C) Autofluorescence of kleptoplasts densely packed under the epidermis and within the mesenchyme. (D) Heterokont kleptoplasts in host cells. (E) Cell junction (small black arrowheads) between two host cells, each containing a heterokont kleptoplast surrounded by at least two membranes (small white arrowheads). l, lipid vesicle; m, mitochondria; n, nucleus; p, plastid; ph, pharynx; py, pyrenoid. Scale bars, 50 (A), 20 (B), 50 (C), and 1 μm (D) and 200 nm (E).

  • Fig. 2 Light, confocal, and transmission electron micrographs of P. paranygulgus and its kleptoplasts.

    (A) Live specimen with eyes (arrow), pharynx, and golden-brown kleptoplasts. (B) Intact (golden brown) and degraded (double black arrowheads) kleptoplasts. (C) Autofluorescence of kleptoplasts in a juvenile specimen; degraded plastids (double white arrowheads) show no autofluorescence. (D and E) Heterokont kleptoplasts adjacent to flatworm mitochondria, lipid droplets and cell junction (arrowheads). Scale bars, 50 (A), 20 (B), 50 (C), 2 (D), and 1 μm (E).

  • Fig. 3 A phylogeny of five partial plastid genes based on transcripts from the transcriptome of B. solaris demonstrates that its kleptoplasts are of diatom origin.

    A concatenated 2956–base pair alignment of psaB, psbA, psbB, atpA, and rbcL was run in MrBayes v3.2.6. Support was assessed with Bayesian posterior probabilities (pp, above branches) and maximum likelihood bootstrap replicates (bs, below branches) from a RAxML analysis. Unsupported branches are collapsed (pp < 0.95) or indicated with a “/” when not supported in RAxML. Scale bar, substitutions/site.

  • Fig. 4 Functional kleptoplasty and short-term retention of plastids in B. solaris is shown by photosynthetic activity and the loss of plastids in starved specimens over time.

    (A) Photosynthetic activity in B. solaris specimens starved for 7 days (n = 25) compared with the chlorophytic alga T. tetrathele (~500,000 cells/ml). Gross photosynthesis was calculated by summing the net photosynthesis and respiration rates. Data represent means ± SE. (B) Plastid retention (proportion of kleptoplastic individuals) and survival rate (proportion of surviving individuals) in filtered seawater (n = 20) and under differential treatments with the photosynthesis inhibitor monolinuron (n = 20 in each treatment). FSW, filtered seawater.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/7/eaaw4337/DC1

    Fig. S1. Freshly collected specimens of B. solaris.

    Fig. S2. Freshly collected specimens of P. paranygulgus.

    Fig. S3. LM and CLSM micrographs of P. paranygulgus.

    Fig. S4. TEM micrographs of B. solaris.

    Fig. S5. Taxonomic partitioning of the transcriptome of B. solaris with BlobTools.

    Fig. S6. Bayesian majority-rule consensus tree of the partial psbA gene recovered from the transcriptome of B. solaris.

    Fig. S7. Bayesian majority-rule consensus tree of the partial psbB gene recovered from the transcriptome of B. solaris.

    Fig. S8. Bayesian majority-rule consensus tree of the partial psaB gene recovered from the transcriptome of B. solaris.

    Fig. S9. Bayesian majority-rule consensus tree of the partial atpA gene recovered from the transcriptome of B. solaris.

    Fig. S10. Bayesian majority-rule consensus tree of the partial rbcL gene recovered from the transcriptome of B. solaris.

    Fig. S11. Bayesian majority-rule consensus tree based on an alignment of rbcL sequences of representative pennate diatoms, PCR-amplified rbcL sequences from the kleptoplasts of different specimens of B. solaris and P. paranygulgus, and rbcL transcripts recovered from the transcriptome of B. solaris.

    Fig. S12. Loss of kleptoplasts in three specimens of B. solaris during the starvation experiment.

    Fig. S13. Busco assessment results of the assembled transcriptome of B. solaris and other publicly available flatworm transcriptomes.

    Table S1. Amplification primers and thermocycling conditions for the partial rbcL gene.

    Table S2. Best-fit partitioning schemes and models of molecular evolution for five plastid genes and the concatenated alignment recovered in PartitionFinder v1.1.0.

    Movie S1. Live adult specimen of B. solaris full of kleptoplasts squeezed under a cover slip.

    Movie S2. Live adult specimen of B. solaris full of kleptoplasts squeezed under a cover slip.

    Movie S3. Compilation of CLSM micrographs showing the autofluorescence of the kleptoplasts in a live juvenile specimen of P. paranygulgus.

    Data file S1. Blastp and blastx annotated transcripts of the plastid-encoded genes, psbA, psbB, atpA, psaB, and rbcL, in the transcriptome of B. solaris are almost exclusively of diatom origin.

    Data file S2. Blastp and blastx annotated transcripts of diatom origin in the transcriptome of B. solaris are all plastid-encoded.

    References (4849)

  • Supplementary Materials

    The PDF file includes:

    • Fig. S1. Freshly collected specimens of B. solaris.
    • Fig. S2. Freshly collected specimens of P. paranygulgus.
    • Fig. S3. LM and CLSM micrographs of P. paranygulgus.
    • Fig. S4. TEM micrographs of B. solaris.
    • Fig. S5. Taxonomic partitioning of the transcriptome of B. solaris with BlobTools.
    • Fig. S6. Bayesian majority-rule consensus tree of the partial psbA gene recovered from the transcriptome of B. solaris.
    • Fig. S7. Bayesian majority-rule consensus tree of the partial psbB gene recovered from the transcriptome of B. solaris.
    • Fig. S8. Bayesian majority-rule consensus tree of the partial psaB gene recovered from the transcriptome of B. solaris.
    • Fig. S9. Bayesian majority-rule consensus tree of the partial atpA gene recovered from the transcriptome of B. solaris.
    • Fig. S10. Bayesian majority-rule consensus tree of the partial rbcL gene recovered from the transcriptome of B. solaris.
    • Fig. S11. Bayesian majority-rule consensus tree based on an alignment of rbcL sequences of representative pennate diatoms, PCR-amplified rbcL sequences from the kleptoplasts of different specimens of B. solaris and P. paranygulgus, and rbcL transcripts recovered from the transcriptome of B. solaris.
    • Fig. S12. Loss of kleptoplasts in three specimens of B. solaris during the starvation experiment.
    • Fig. S13. Busco assessment results of the assembled transcriptome of B. solaris and other publicly available flatworm transcriptomes.
    • Table S1. Amplification primers and thermocycling conditions for the partial rbcL gene.
    • Table S2. Best-fit partitioning schemes and models of molecular evolution for five plastid genes and the concatenated alignment recovered in PartitionFinder v1.1.0.
    • Legends for movies S1 to S3
    • Legends for data files S1 and S2
    • References (4849)

    Download PDF

    Other Supplementary Material for this manuscript includes the following:

    • Movie S1 (.mov format). Live adult specimen of B. solaris full of kleptoplasts squeezed under a cover slip.
    • Movie S2 (.mov format). Live adult specimen of B. solaris full of kleptoplasts squeezed under a cover slip.
    • Movie S3 (.mov format). Compilation of CLSM micrographs showing the autofluorescence of the kleptoplasts in a live juvenile specimen of P. paranygulgus.
    • Data file S1 (Microsoft Excel format). Blastp and blastx annotated transcripts of the plastid-encoded genes, psbA, psbB, atpA, psaB, and rbcL, in the transcriptome of B. solaris are almost exclusively of diatom origin.
    • Data file S2 (Microsoft Excel format). Blastp and blastx annotated transcripts of diatom origin in the transcriptome of B. solaris are all plastid-encoded.

    Files in this Data Supplement:

Navigate This Article