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. 2016 Aug 24:4:e2358.
doi: 10.7717/peerj.2358. eCollection 2016.

Transmission of a heterologous clade C Symbiodinium in a model anemone infection system via asexual reproduction

Wan-Nan U Chen  1 , Ya-Ju Hsiao  2 , Anderson B Mayfield  3 , Ryan Young  4 , Ling-Lan Hsu  5 , Shao-En Peng  6
Affiliations

Transmission of a heterologous clade C Symbiodinium in a model anemone infection system via asexual reproduction

Wan-Nan U Chen et al. PeerJ. .

Abstract

Anemones of genus Exaiptasia are used as model organisms for the study of cnidarian-dinoflagellate (genus Symbiodinium) endosymbiosis. However, while most reef-building corals harbor Symbiodinium of clade C, Exaiptasia spp. anemones mainly harbor clade B Symbiodinium (ITS2 type B1) populations. In this study, we reveal for the first time that bleached Exaiptasia pallida anemones can establish a symbiotic relationship with a clade C Symbiodinium (ITS2 type C1). We further found that anemones can transmit the exogenously supplied clade C Symbiodinium cells to their offspring by asexual reproduction (pedal laceration). In order to corroborate the establishment of stable symbiosis, we used microscopic techniques and genetic analyses to examine several generations of anemones, and the results of these endeavors confirmed the sustainability of the system. These findings provide a framework for understanding the differences in infection dynamics between homologous and heterologous dinoflagellate types using a model anemone infection system.

Keywords: Endosymbiology; Marine biology; Microalgae.

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Conflict of interest statement

The authors declare there are no competing interests.

Figures

Figure 1
Figure 1. A representative bleached and a representative clade C Symbiodinium-infected anemone and its lacerates.
(A) Representative image of a bleached anemone that had lost its brownish coloration following the expulsion of Symbiodinium cells during cold shock-induced bleaching. (B) Aboral view of a representative clade C Symbiodinium-infected anemone showing brownish Symbiodinium cells distributed throughout the body, with a notable degree of dinoflagellate aggregation in the margins of the pedal disk (arrow), as well as within the newly budded lacerates (triangles). Scale bars: 0.5 cm.
Figure 2
Figure 2. Development of a representative lacerate collected from a clade C Symbiodinium-infected anemone.
First, the lacerate was transferred to a new dish immediately following laceration from the pedal disk of a clade C Symbiodinium-infected anemone. The development of the lacerate and spread of Symbiodinium was recorded daily using a fluorescent stereomicroscope (A–I). The red spots in the images indicate chlorophyll autofluorescence of the Symbiodinium cells. Scale bars: 100 µm.
Figure 3
Figure 3. Images of the clade C Symbiodinium-infected anemones and their offspring.
(A) Generation 1 (G1) anemones maintained in the laboratory for more than one year; (B) Generation 2 (G2) anemones cultured for more than three months; (C) Generation 3 (G3) of anemone cultured for 15 days following laceration. Scale bar: 1 cm.
Figure 4
Figure 4. Restriction fragment length polymorphism (RFLP) analysis of three generations of the clade C Symbiodinium-infected anemones.
Amplified genomic fragments of small subunit ribosomal RNA genes (18S rDNA) from Symbiodinium were digested using the restriction enzymes TaqI and Sau3A I (A and B, respectively). Lane 1 (control): Normal anemone harboring clade B Symbiodinium. Lanes 2–4: Generation 1 (G1) anemones. Lanes 5–7: Generation 2 (G2) anemones. Lanes 8–10: Generation 3 (G3) anemones. Ep, Exaiptasia pallida; MW, molecular weight.
Figure 5
Figure 5. The morphology of clade B and clade C Symbiodinium cells within their host anemone tissue.
(A) Tentacular tissues harboring clade B Symbiodinium; (B) Tentacular tissues harboring clade C Symbiodinium. Scale bar: 20 µm.
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Grants and funding

This work was supported by grants from Taiwan’s Ministry of Science and Technology (NSC 102-2311-B-291-002-MY3 to WNUC; NSC 102-2311-B-291-001 & MOST 103-2311-B-291-001-MY3 to SEP), as well as intramural funding from the National Museum of Marine Biology and Aquarium. ABM was supported by a postdoctoral research fellowship from the Khaled bin Sultan Living Oceans Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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